Molecular Cloning of a Novel Laminin Chain, alpha5, and Widespread Expression in Adult Mouse Tissues

doi:10.1074/jbc.270.48.28523

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Volume 270, Number 48, Issue of December 1, 1995 pp. 28523-28526
©1995 by The American Society for Biochemistry and Molecular Biology, Inc.

Molecular Cloning of a Novel Laminin Chain, 5, and Widespread Expression in Adult Mouse Tissues (*)

(Received for publication, September 27, 1995)

Jeffrey H. Miner (§), , Renate M. Lewis , Joshua R. Sanes (¶)

From the Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110

ABSTRACT

INTRODUCTION

MATERIALS AND METHODS

RESULTS AND DISCUSSION

FOOTNOTES

ACKNOWLEDGEMENTS

REFERENCES

ABSTRACT

We have identified a fifth member of the alpha subfamily of vertebrate laminin chains. Sequence analysis revealed a close relationship of alpha 5 to the only known Drosophila alpha chain, suggesting that the ancestral alpha gene was more similar to alpha 5 than to alpha 1-4. Analysis of RNA expression showed that alpha 5 is widely expressed in adult tissues, with highest levels in lung, heart, and kidney. Our results suggest that alpha 5 may be a major laminin chain of adult basal laminae.

INTRODUCTION

Laminins are major glycoproteins of basal laminae throughout the vertebrate body. Originally identified as structural components, it is now clear that laminins are also signaling molecules that regulate the proliferation, motility, and differentiation of the cells they contact (1, 2, 3) . The first laminin discovered(4, 5) , now called laminin-1(6) , is a trimer of related A, B1, and B2 chains(7, 8, 9) . The subsequent discovery of the novel laminin chains S-laminin (10) and merosin-M (11) revealed that the laminins comprised a larger gene family than initially envisioned. More recently, four additional chains have been cloned(12, 13, 14, 15, 16, 17, 18, 19) . So far, however, all laminin chains sequenced resemble either A, B1, or B2, and all of the laminins purified are trimers containing an A-like, a B1-like, and a B2-like chain(6, 19, 20, 21, 22) . Based on these findings, a new nomenclature has been adopted in which laminin chains are divided into alpha (A-like), beta (B1-like) and (B2-like) subfamilies; A, M, B1, S, and B2 are now called alpha 1, alpha 2, beta 1, beta 2, and 1, respectively(6) .

Consistent with laminin's trimeric structure, all basal laminae characterized to date contain at least one beta and at least one chain(19, 20, 23, 24, 25, 26, 27, 28) . For the alpha chains, on the other hand, the situation is less clear. For example, perineurial basal lamina in peripheral nerve stained poorly with anti- alpha 1 and not at all with anti- alpha 2(23) . Likewise, in kidney, glomerular basement membrane was alpha 2-negative and reacted only moderately well (in human(23) ) or not at all (in mouse(29, 30) ) with anti- alpha 1. If all laminins are alpha / beta / trimers, these results imply that additional laminin alpha chains exist. Indeed, several biochemical studies have provided evidence for an alpha -like laminin chain distinct from alpha 1 and alpha 2 (31, 32, 33) . The recent discoveries of the alpha 3 and alpha 4 chains(15, 16, 17, 18) are provocative in this context, but we ()and others (16, 18) found little alpha 3 or alpha 4 in several tissues with alpha 1- and alpha 2-negative basal laminae.

Accordingly, we undertook a search for additional laminin alpha chains. Using the polymerase chain reaction, we have identified laminin alpha 5, a novel murine alpha chain. Sequence analysis reveals that alpha 5 is more similar in domain structure to Drosophila laminin A(34, 35) than it is to mammalian alpha 1-4; the ancestral vertebrate alpha chain may, therefore, have been more similar to alpha 5 that to alpha 1-4. RNA analysis demonstrates that alpha 5 is widely expressed in adult tissues and thus may be a major laminin alpha chain of adult basal laminae.

MATERIALS AND METHODS

Degenerate primers were designed based on sequences conserved between mouse laminin alpha 1 (7) and human laminin alpha 2(36) . Reverse transcription-PCR ()was performed on RNA from postnatal day 7 mouse kidney using a GeneAmp kit (Perkin-Elmer). One pair of primers from the amino terminus of domain V (sense, 5`-GGNAGTTGYATHTGYTAYGGNC-3` and antisense, 5`-TRCANTGYTCRCARTTDATNCC-3`, where N = A/G/C/T, H = A/T/C, and D = G/A/T) produced a fragment of appropriate length (330 base pairs). The band was excised from agarose (SeaPlaque GTG, FMC Bioproducts, Rockland, ME), reamplified with the same primers, purified with a Wizard PCR Preps kit (Promega Corp., Madison, WI), and incubated with BglI to digest laminin alpha 1 products, thereby preventing their further amplification. The remaining full-length product was reamplified and ligated into the pCRII vector (Invitrogen Corp., San Diego, CA).

One resulting clone, DB2, bore an insert related to but distinct from laminins alpha 1 and alpha 2. The DB2 insert was labeled with [P]dCTP by the random primed DNA labeling kit (Boehringer Mannheim) and used to screen an adult mouse lung oligo(dT)+ random primed ZAP II cDNA library (Stratagene, La Jolla, CA). Subsequent cDNA library screening was performed as a ``walk'' using selected restriction fragments of hybridizing phage to obtain overlapping clones. Clones were sequenced on an ABI 373A DNA sequencer using a Taq DyeDeoxy Terminator cycle sequencing kit (Applied Biosystems Inc., Foster City, CA). All sequences were determined from both strands. Data base homology searches were performed on the BLAST server at the National Center for Biotechnology Information(37) , and sequences were compared using Genetics Computing Group programs(38) .

For Northern analysis, a filter containing poly(A)-selected RNA from several adult mouse tissues (Clontech) was hybridized with a probe comprising nucleotides 7855-9361 of the alpha 5 sequence. RNase protection analysis was performed as described previously(24) .

RESULTS AND DISCUSSION

Molecular Cloning of Laminin 5

We used PCR to amplify a 334-base pair fragment from mouse kidney that encoded a novel laminin-like sequence. This fragment was used as the starting point for isolation of a series of overlapping cDNA clones that spanned >11 kb. Sequence analysis revealed that the cDNAs encoded a single open reading frame of 3610 amino acids (Fig. 1). The sequence of the predicted protein is related to but clearly distinct from those of previously reported laminin chains(7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 34, 35, 36) . As detailed below, the novel sequence is more closely related to laminin alpha

chains than to beta

chains. Because four mammalian laminin alpha

chains have been described to date(7, 11, 15, 16, 17, 18) , we have named the novel chain laminin alpha

Figure 1: Amino acid sequence of the mouse laminin alpha 5 chain, deduced from cDNAs. Domain boundaries are noted and the adhesive tripeptide sequences, RGD (40) and LRE(42) , are indicated by bullets. The nucleotide sequence is available from GenBank under accession number U37501.

The first amino acid of the deduced sequence is aspartic acid rather than methionine, indicating that the cDNAs do not reach the 5` end of the coding sequence. Repeated efforts to obtain additional cDNAs failed. Based on homology to other laminin alpha chains, we believe that the mature protein contains 3630 amino acids, of which we have identified 3610.

Comparison with Other Laminin Chains

The laminin alpha

5 chain contains eight domains, based on predicted secondary structure and homology to the laminin alpha

1 chain (Fig. 2A). Their nomenclature follows that for alpha

1, which was in turn designed to maintain consistency with the beta

1 and

1 chains(1, 7) . The carboxyl-terminal half of the protein contains a large (

100 kDa) globular domain (G) and an alpha

-helical segment (I/II). The amino-terminal half contains three cysteine- and glycine-rich regions predicted to form rigid, rodlike structures (IIIa, IIIb, and V) and three smaller globular regions (IVa, IVb, and VI). Five of the domains are characterized by repeating structures: heptad repeats with hydrophobic residues in the first and fourth position of domain I/II; ``EGF-like'' repeats of

50 amino acids each in domains IIIa, IIIb, and V; and five tandem ``G'' repeats of

186 amino acids each in G.

Figure 2: Relationship of alpha 5 to other laminin chains. A, domain structure of the known laminin alpha chains. The names of the domains, based on accepted nomenclature(1, 7) , are to the left of alpha 5. Percent amino acid identity of individual domains of alpha 5 with the corresponding domains of the other alpha chains, determined with the GAP program(38) , is shown to the left of the other alpha chains. Numbers of EGF repeats, rounded to the nearest integer, are indicated within domains III and V. Domain structures of beta 1 and 1 are shown to indicate the basis for assigning alpha 5 to the alpha subfamily. alpha D, Drosophila A. B, relationships among mammalian and Drosophila alpha chains, based on sequence alignment performed by the PILEUP program(38) . Comparisons were based on domains G-IIIa, which all alpha chains contain. C, evolutionary scheme for vertebrate alpha chains, incorporating comparisons of primary sequences (from B) and predicted secondary structure (from A). In this scheme, the ancestral alpha gene was more similar in domain structure to alpha 5 than to alpha 1-4. See text for details.

Several features of alpha 5 identify it as an alpha chain (Fig. 2A). First, it contains a G domain, which is present in all alpha but no beta or chains. Second, alpha 5, like alpha 1 and alpha 2, contains three sets of EGF-like repeats (IIIa, IIIb, and V) and three globular regions (IVa, IVb, and VI) in its amino-terminal half, whereas no beta or chain has more than two of each. Third, alpha 5 lacks the alpha -insert between domains I and II that characterizes beta chains.

Of the four vertebrate laminin alpha chains characterized to date, two ( alpha 1 and alpha 2) contain domains G-VI, whereas the other two ( alpha 3 and alpha 4) are truncated and contain only domains G-IIIa (Fig. 2A). An alternatively spliced product of the alpha 3 gene, alpha 3B, which contains domains IIIb and IV, has been identified but not yet fully sequenced(12) . In its domain structure, alpha 5 is more similar to alpha 1 and alpha 2 than to alpha 3 or alpha 4, and it can therefore be classified as a ``full-length'' alpha chain. On the other hand, within the domains shared by all alpha chains, the laminin alpha 5 sequence is more similar to alpha 3 and alpha 4 than to alpha 1 or alpha 2 (Fig. 2B). Thus, sequence analysis reveals an apparent discrepancy between relationships based on primary and secondary structure.

More surprising is that alpha 5 is more similar in domain structure to the only known Drosophila A chain ( alpha D(34, 35) ) than it is to any of the vertebrate alpha chains. Both alpha 5 and alpha D contain 11 EGF repeats in domain V, 4 in domain IIIb, and 7 in domain IIIa, whereas alpha 1 and alpha 2 have 4, 9, and 4 repeats in domains V, IIIb, and IIIa, respectively (Fig. 2A). Likewise, domain IVb is much larger in alpha D and alpha 5 (558 and 577 amino acids) than in alpha 1 or alpha 2 (196 amino acids).

Together, these results suggest the evolutionary scheme diagrammed in Fig. 2C. We propose than an ancestral alpha gene, similar in domain structure to alpha D and alpha 5, was duplicated early in the vertebrate lineage. One of the daughter genes evolved the alpha 1/2 domain structure, perhaps by recombination(39) , and was then duplicated again to generate alpha 1 and alpha 2. The other product of the original duplication was also reduplicated. One daughter evolved into alpha 5 without further rearrangement, while the other suffered truncation and then duplicated yet again to generate alpha 3 and alpha 4. Although speculative, this scheme accounts for the otherwise puzzling findings that alpha 5 resembles alpha 1 and alpha 2 in secondary structure but is most closely related to alpha 3 and alpha 4 in primary sequence.

Studies with synthetic peptides have provided evidence for several discrete adhesive sites within laminin alpha chains, although their significance in vivo remains unclear. The tripeptide RGD, which is recognized by several integrins(40) , is present in alpha 1, alpha 3, and alpha 4 but not in alpha 2 or alpha D(7, 15, 18, 34, 35, 36, 41) ; it is present twice within the alpha 5 sequence (Fig. 1). The tripeptide LRE, a major determinant of a motoneuron-selective adhesive site in beta 2(42, 43) , is present in alpha 1, alpha 3, and alpha D but not in alpha 2 or alpha 4(7, 15, 18, 34, 35, 36, 41) ; it is present twice in alpha 5. Finally, the sequence IKVAV, an adhesive site in alpha 1(44) , is replaced by SKVKV in alpha 5.

Expression of Laminin 5

RNA from a panel of adult mouse tissues was subjected to Northern analysis with an alpha

5 cDNA. High levels of alpha

5 mRNA were detected in heart, lung, and kidney (Fig. 3A). Longer exposures revealed lower but significant levels of alpha

5 mRNA in brain, muscle, and testis (Fig. 3B). In all of these tissues, an RNA species of

12 kb was detected; an additional RNA of 9 kb, visible only in testis, would be unable to encode full-length alpha

5. A more sensitive RNase protection assay revealed significant levels of alpha

5 RNA in liver, as well as in gut and skin (not shown). Moreover, RNase protection and in situ hybridization analyses indicated that alpha

5 is expressed in many tissues by embryonic day 11. (

)Thus, the alpha

5 gene is widely expressed.

Figure 3: Northern analysis of laminin alpha 5 RNA from adult mouse tissues. Short (15 h (A)) and long (52 h (B)) exposures of a single blot (with an intensifying screen) are shown.

The broad distribution of alpha 5 RNA in adult tissues stands in marked contrast to the restricted patterns of expression of the alpha 1, alpha 3, and alpha 4 genes(16, 18, 30, 41) . ()Laminin alpha 2 RNA is widely distributed in adult tissues but is predominantly expressed by mesenchymal or mesodermal cells(36) . Taken together, these results suggest that laminin alpha 5 is a major alpha chain of adult epithelial and/or endothelial basal laminae. Moreover, it seems possible that reports of alpha 1-like immunoreactivity in tissues such as kidney, lung, and muscle(20, 23, 25, 26, 27, 28) , which contain little alpha 1 RNA, reflect cross-reactivity of anti- alpha 1 antibodies with alpha 5. We are currently preparing monospecific antibodies to evaluate this possibility.

FOOTNOTES

*

This work was supported by a National Institutes of Health grant. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore by hereby marked ``advertisement'' in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank(TM)/EMBL Data Bank with accession number(s) U37501[GenBank].

§

Supported by a fellowship from the Damon Runyon-Walter Winchell Cancer Research Fund.

¶

To whom correspondence should be addressed: Dept. of Anatomy and Neurobiology, Washington University School of Medicine, 660 South Euclid Ave., Box 8108, St. Louis, MO 63110. Tel.: 314-362-2507; Fax: 314-747-1150; sanesj@thalamus.wustl.edu.

()

J. H. Miner, J. R. Sanes, and D. Aberdam, unpublished data.

()

The abbreviations used are: PCR, polymerase chain reaction; kb, kilobase(s); EGF, epidermal growth factor.

()

J. H. Miner, S. I. Lentz, W. D. Snider, and J. R. Sanes, manuscript in preparation.

()

J. H. Miner, unpublished results.

ACKNOWLEDGEMENTS

We thank Guoping Feng and Jacqueline Mudd for advice and assistance.

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[Abstract] [Full Text] [PDF]

H. Ido, K. Harada, S. Futaki, Y. Hayashi, R. Nishiuchi, Y. Natsuka, S. Li, Y. Wada, A. C. Combs, J. M. Ervasti, et al.
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[Abstract] [Full Text] [PDF]

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[Abstract] [Full Text] [PDF]

C.-c. Huang, D. H. Hall, E. M. Hedgecock, G. Kao, V. Karantza, B. E. Vogel, H. Hutter, A. D. Chisholm, P. D. Yurchenco, and W. G. Wadsworth
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T. L. Adair-Kirk, J. J. Atkinson, T. J. Broekelmann, M. Doi, K. Tryggvason, J. H. Miner, R. P. Mecham, and R. M. Senior
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Y. Kikkawa, I. Virtanen, and J. H. Miner
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Y.-C. Gu, J. Kortesmaa, K. Tryggvason, J. Persson, P. Ekblom, S.-E. Jacobsen, and M. Ekblom
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[Abstract] [Full Text] [PDF]

S. K. Chintala, X. Zhang, J. S. Austin, and M. E. Fini
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[Abstract] [Full Text] [PDF]

Y. Kikkawa, C. L. Moulson, I. Virtanen, and J. H. Miner
Identification of the Binding Site for the Lutheran Blood Group Glycoprotein on Laminin alpha 5 through Expression of Chimeric Laminin Chains in Vivo
J. Biol. Chem., November 15, 2002; 277(47): 44864 - 44869.
[Abstract] [Full Text] [PDF]

M. E. Lauer and K. J. McCarthy
In Vitro Matrix Assembly Induced by Critical Assembly Concentration (CAC)
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L. Lin and M. Kurpakus-Wheater
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J. Gu, A. Fujibayashi, K. M. Yamada, and K. Sekiguchi
Laminin-10/11 and Fibronectin Differentially Prevent Apoptosis Induced by Serum Removal via Phosphatidylinositol 3-Kinase/Akt- and MEK1/ERK-dependent Pathways
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[Abstract] [Full Text] [PDF]

M. Doi, J. Thyboll, J. Kortesmaa, K. Jansson, A. Iivanainen, M. Parvardeh, R. Timpl, U. Hedin, J. Swedenborg, and K. Tryggvason
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Endothelial Cell Laminin Isoforms, Laminins 8 and 10, Play Decisive Roles in T Cell Recruitment Across the Blood-Brain Barrier in Experimental Autoimmune Encephalomyelitis
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[Abstract] [Full Text] [PDF]

R. A. Pierce, G. L. Griffin, J. H. Miner, and R. M. Senior
Expression Patterns of Laminin alpha 1 and alpha 5 in Human Lung during Development
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[Abstract] [Full Text]

C. Pedraza, T. Geberhiwot, S. Ingerpuu, D. Assefa, Z. Wondimu, J. Kortesmaa, K. Tryggvason, I. Virtanen, and M. Patarroyo
Monocytic Cells Synthesize, Adhere to, and Migrate on Laminin-8 ({alpha}4{beta}1{gamma}1)
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[Abstract] [Full Text] [PDF]

A. C. Erickson and J. R. Couchman
Still More Complexity in Mammalian Basement Membranes
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[Abstract] [Full Text]

R. T. Libby, M.-F. Champliaud, T. Claudepierre, Y. Xu, E. P. Gibbons, M. Koch, R. E. Burgeson, D. D. Hunter, and W. J. Brunken
Laminin Expression in Adult and Developing Retinae: Evidence of Two Novel CNS Laminins
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[Abstract] [Full Text] [PDF]

J. Kortesmaa, P. Yurchenco, and K. Tryggvason
Recombinant Laminin-8 (alpha 4beta 1gamma 1). PRODUCTION, PURIFICATION, AND INTERACTIONS WITH INTEGRINS
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[Abstract] [Full Text] [PDF]

H. Hutter, B. E. Vogel, J. D. Plenefisch, C. R. Norris, R. B. Proenca, J. Spieth, C. Guo, S. Mastwal, X. Zhu, I. S. A. J. Scheel, et al.
Conservation and Novelty in the Evolution of Cell Adhesion and Extracellular Matrix Genes
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Y.-J. Son, T. W. Scranton, W. J. Sunderland, S. J. Baek, J. H. Miner, J. R. Sanes, and S. S. Carlson
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Y Kikkawa, N Sanzen, H Fujiwara, A Sonnenberg, and K Sekiguchi
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[Abstract] [PDF]

T.-S. HA, J. L. BARNES, J. L. STEWART, C. W. KO, J. H. MINER, D. R. ABRAHAMSON, J. R. SANES, and B. S. KASINATH
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[Abstract] [Full Text]

A. Iivanainen, T. Morita, and K. Tryggvason
Molecular Cloning and Tissue-specific Expression of a Novel Murine Laminin gamma 3 Chain
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[Abstract] [Full Text] [PDF]

M. Koch, P. F. Olson, A. Albus, W. Jin, D. D. Hunter, W. J. Brunken, R. E. Burgeson, and M.-F. Champliaud
Characterization and Expression of the Laminin gamma 3 Chain: A Novel, Non-Basement Membrane-associated, Laminin Chain
J. Cell Biol., May 3, 1999; 145(3): 605 - 618.
[Abstract] [Full Text] [PDF]

H. Shimizu, H. Hosokawa, H. Ninomiya, J. H. Miner, and T. Masaki
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[Abstract] [Full Text] [PDF]

Y. Gu, L. Sorokin, M. Durbeej, T. Hjalt, J.-I. Jonsson, and M. Ekblom
Characterization of Bone Marrow Laminins and Identification of alpha 5-Containing Laminins as Adhesive Proteins for Multipotent Hematopoietic FDCP-Mix Cells
Blood, April 15, 1999; 93(8): 2533 - 2542.
[Abstract] [Full Text] [PDF]

J. H. Miner, J. Cunningham, and J. R. Sanes
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[Abstract] [Full Text] [PDF]

S. P. Lee, M. L. Cunningham, P. C. Hines, C. C. Joneckis, E. P. Orringer, and L. V. Parise
Sickle Cell Adhesion to Laminin: Potential Role for the alpha 5 Chain
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[Abstract] [Full Text] [PDF]

E. L. McDearmon, A. L. Burwell, A. C. Combs, B. A. Renley, M. T. Sdano, and J. M. Ervasti
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[Abstract] [Full Text] [PDF]

R. A. Pierce, G. L. Griffin, M. Susan Mudd, M. A. Moxley, W. J. Longmore, J. R. Sanes, J. H. Miner, and R. M. Senior
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[Abstract] [Full Text]

M. W. Graner, T. A. Bunch, S. Baumgartner, A. Kerschen, and D. L. Brower
Splice Variants of the Drosophila PS2 Integrins Differentially Interact with RGD-containing Fragments of the Extracellular Proteins Tiggrin, Ten-m, and D-Laminin alpha 2
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[Abstract] [Full Text] [PDF]

S. M. Culican, C. C. Nelson, and J. W. Lichtman
Axon Withdrawal during Synapse Elimination at the Neuromuscular Junction Is Accompanied by Disassembly of the Postsynaptic Specialization and Withdrawal of Schwann Cell Processes
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[Abstract] [Full Text] [PDF]

Y. Kikkawa, N. Sanzen, and K. Sekiguchi
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[Abstract] [Full Text] [PDF]

M. Durbeej, M. D. Henry, M. Ferletta, K. P. Campbell, and P. Ekblom
Distribution of Dystroglycan in Normal Adult Mouse Tissues
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[Abstract] [Full Text]

A. J. Groffen, M. A. Ruegg, H. Dijkman, T. J. van de Velden, C. A. Buskens, J. van den Born, K. J. Assmann, L. A. Monnens, J. H. Veerkamp, and L. P. van den Heuvel
Agrin Is a Major Heparan Sulfate Proteoglycan in the Human Glomerular Basement Membrane
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[Abstract] [Full Text]

Y.-S. Cheng, M.-F. Champliaud, R. E. Burgeson, M. P. Marinkovich, and P. D. Yurchenco
Self-assembly of Laminin Isoforms
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[Abstract] [Full Text] [PDF]

C.-F. Tiger, M.-F. Champliaud, F. Pedrosa-Domellof, L.-E. Thornell, P. Ekblom, and D. Gullberg
Presence of Laminin alpha 5 Chain and Lack of Laminin alpha 1 Chain during Human Muscle Development and in Muscular Dystrophies
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[Abstract] [Full Text] [PDF]

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[Abstract] [Full Text] [PDF]

L. Schuger, A. P.N. Skubitz, J. Zhang, L. Sorokin, and L. He
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[Abstract] [Full Text] [PDF]

J. H. Miner, B. L. Patton, S. I. Lentz, D. J. Gilbert, W. D. Snider, N. A. Jenkins, N. G. Copeland, and J. R. Sanes
The Laminin alpha �Chains: Expression, Developmental Transitions, and Chromosomal Locations of alpha 1-5, Identification of Heterotrimeric Laminins 8-11, and Cloning of a Novel alpha 3 Isoform
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[Abstract] [Full Text] [PDF]

R.-R. Wu and J. R. Couchman
cDNA Cloning of the Basement Membrane Chondroitin Sulfate Proteoglycan Core Protein, Bamacan: A Five Domain Structure Including Coiled-Coil Motifs
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[Abstract] [Full Text] [PDF]

X. Zhang, R. Vuolteenaho, and K. Tryggvason
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[Abstract] [Full Text] [PDF]

Y. Takagi, M. Nomizu, D. Gullberg, A. J. MacKrell, D. R. Keene, Y. Yamada, and J. H. Fessler
Conserved Neuron Promoting Activity in Drosophila and Vertebrate Laminin alpha 1
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[Abstract] [Full Text] [PDF]

M. E. Durkin, M. Gautam, F. Loechel, J. R. Sanes, J. P. Merlie, R. Albrechtsen, and U. M. Wewer
Structural Organization of the Human and Mouse Laminin beta 2 Chain Genes, and Alternative Splicing at the 5' End of the Human Transcript
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[Abstract] [Full Text] [PDF]

H. Yamaguchi, H. Yamashita, H. Mori, I. Okazaki, M. Nomizu, K. Beck, and Y. Kitagawa
High and Low Affinity Heparin-binding Sites in the G Domain of the Mouse Laminin alpha 4 Chain
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[Abstract] [Full Text] [PDF]

L. E. Goldfinger, L. Jiang, S. B. Hopkinson, M. S. Stack, and J. C. R. Jones
Spatial Regulation and Activity Modulation of Plasmin by High Affinity Binding to the G domain of the alpha 3 Subunit of Laminin-5
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[Abstract] [Full Text] [PDF]

P. K. Nielsen and Y. Yamada
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[Abstract] [Full Text] [PDF]

J. Gu, Y. Sumida, N. Sanzen, and K. Sekiguchi
Laminin-10/11 and Fibronectin Differentially Regulate Integrin- dependent Rho and Rac Activation via p130Cas-CrkII-DOCK180 Pathway
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[Abstract] [Full Text] [PDF]

N. M. Nguyen, Y. Bai, K. Mochitate, and R. M. Senior
Laminin alpha -chain expression and basement membrane formation by MLE-15 respiratory epithelial cells
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