Journal Article
. 2012 Jun; 7(6):e39097.
doi: 10.1371/journal.pone.0039097.

The heterotrimeric laminin coiled-coil domain exerts anti-adhesive effects and induces a pro-invasive phenotype

Patricia Santos-Valle 1 Irene Guijarro-Muñoz  Angel M Cuesta  Vanesa Alonso-Camino  Maider Villate  Ana Alvarez-Cienfuegos  Francisco J Blanco  Laura Sanz  Luis Alvarez-Vallina  
Affiliations
  • PMID: 22723936
  •     45 References
  •     7 citations

Abstract

Laminins are large heterotrimeric cross-shaped extracellular matrix glycoproteins with terminal globular domains and a coiled-coil region through which the three chains are assembled and covalently linked. Laminins are key components of basement membranes, and they serve as attachment sites for cell adhesion, migration and proliferation. In this work, we produced a recombinant fragment comprising the entire laminin coiled-coil of the α1-, β1-, and γ1-chains that assemble into a stable heterotrimeric coiled-coil structure independently of the rest of the molecule. This domain was biologically active and not only failed to serve as a substrate for cell attachment, spreading and focal adhesion formation but also inhibited cell adhesion to laminin when added to cells in a soluble form at the time of seeding. Furthermore, gene array expression profiling in cells cultured in the presence of the laminin coiled-coil domain revealed up-regulation of genes involved in cell motility and invasion. These findings were confirmed by real-time quantitative PCR and zymography assays. In conclusion, this study shows for the first time that the laminin coiled-coil domain displays anti-adhesive functions and has potential implications for cell migration during matrix remodeling.

Interaction of agrin with laminin requires a coiled-coil conformation of the agrin-binding site within the laminin gamma1 chain.
R A Kammerer, T Schulthess, +6 authors, A J Denzer.
EMBO J, 1999 Dec 03; 18(23). PMID: 10581249    Free PMC article.
Assembly of synthetic laminin peptides into a triple-stranded coiled-coil structure.
M Nomizu, A Otaka, +2 authors, Y Yamada.
J Biol Chem, 1994 Dec 02; 269(48). PMID: 7982952
Proteolytic processing of laminin-5 by MT1-MMP in tissues and its effects on epithelial cell morphology.
Naohiko Koshikawa, Susann Schenk, +5 authors, Vito Quaranta.
FASEB J, 2003 Dec 23; 18(2). PMID: 14688206
Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats.
M Sasaki, S Kato, +2 authors, Y Yamada.
Proc Natl Acad Sci U S A, 1987 Feb 01; 84(4). PMID: 3493487    Free PMC article.
Highly Cited.
Mechanism of laminin chain assembly into a triple-stranded coiled-coil structure.
M Nomizu, A Utani, +3 authors, Y Yamada.
Biochemistry, 1996 Mar 05; 35(9). PMID: 8608125
Extracellular matrix-induced gene expression in human breast cancer cells.
Nandor Garamszegi, Susanna P Garamszegi, Lina A Shehadeh, Sean P Scully.
Mol Cancer Res, 2009 Mar 12; 7(3). PMID: 19276183    Free PMC article.
Matrilysin 1 influences colon carcinoma cell migration by cleavage of the laminin-5 beta3 chain.
Lionel Remy, Cécile Trespeuch, +2 authors, Patricia Rousselle.
Cancer Res, 2006 Dec 06; 66(23). PMID: 17145868
Formation of hyaluronan- and versican-rich pericellular matrix by prostate cancer cells promotes cell motility.
Carmela Ricciardelli, Darryl L Russell, +6 authors, David J Horsfall.
J Biol Chem, 2007 Feb 13; 282(14). PMID: 17293599
The extracellular matrix: a new turn-of-the-screw for anti-angiogenic strategies.
Laura Sanz, Luis Alvarez-Vallina.
Trends Mol Med, 2003 Jun 28; 9(6). PMID: 12829014
Self-assembly and calcium-binding sites in laminin. A three-arm interaction model.
P D Yurchenco, Y S Cheng.
J Biol Chem, 1993 Aug 15; 268(23). PMID: 8349613
Highly Cited.
The alpha chain of laminin-1 is independently secreted and drives secretion of its beta- and gamma-chain partners.
P D Yurchenco, Y Quan, +4 authors, J J O'Rear.
Proc Natl Acad Sci U S A, 1997 Sep 18; 94(19). PMID: 9294185    Free PMC article.
Role of laminin terminal globular domains in basement membrane assembly.
Karen K McKee, David Harrison, Stephanie Capizzi, Peter D Yurchenco.
J Biol Chem, 2007 May 23; 282(29). PMID: 17517882
pH-induced folding of an apoptotic coiled coil.
K Dutta, A Alexandrov, H Huang, S M Pascal.
Protein Sci, 2001 Nov 21; 10(12). PMID: 11714921    Free PMC article.
Cell binding sequences in mouse laminin alpha1 chain.
M Nomizu, Y Kuratomi, +7 authors, Y Yamada.
J Biol Chem, 1998 Nov 26; 273(49). PMID: 9829982
Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5.
G Giannelli, J Falk-Marzillier, +2 authors, V Quaranta.
Science, 1997 Jul 11; 277(5323). PMID: 9211848
Highly Cited.
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository.
Ron Edgar, Michael Domrachev, Alex E Lash.
Nucleic Acids Res, 2001 Dec 26; 30(1). PMID: 11752295    Free PMC article.
Highly Cited.
Recombinant laminin-8 (alpha(4)beta(1)gamma(1)). Production, purification,and interactions with integrins.
J Kortesmaa, P Yurchenco, K Tryggvason.
J Biol Chem, 2000 May 16; 275(20). PMID: 10809728
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.
Da Wei Huang, Brad T Sherman, Richard A Lempicki.
Nat Protoc, 2009 Jan 10; 4(1). PMID: 19131956
Highly Cited.
Use of real-time quantitative PCR to validate the results of cDNA array and differential display PCR technologies.
M S Rajeevan, D G Ranamukhaarachchi, S D Vernon, E R Unger.
Methods, 2002 Feb 16; 25(4). PMID: 11846613
Exploration, normalization, and summaries of high density oligonucleotide array probe level data.
Rafael A Irizarry, Bridget Hobbs, +4 authors, Terence P Speed.
Biostatistics, 2003 Aug 20; 4(2). PMID: 12925520
Highly Cited.
Cell and heparin binding in the distal long arm of laminin: identification of active and cryptic sites with recombinant and hybrid glycoprotein.
U Sung, J J O'Rear, P D Yurchenco.
J Cell Biol, 1993 Dec 01; 123(5). PMID: 8267779    Free PMC article.
Tumour suppressor function of MDA-7/IL-24 in human breast cancer.
Neill Patani, Anthony Douglas-Jones, +2 authors, Kefah Mokbel.
Cancer Cell Int, 2010 Aug 26; 10. PMID: 20735832    Free PMC article.
Expression of osteopontin coregulators in primary colorectal cancer and associated liver metastases.
D J Mole, C O'Neill, +6 authors, F C Campbell.
Br J Cancer, 2011 Feb 24; 104(6). PMID: 21343932    Free PMC article.
The E8 subfragment of laminin promotes locomotion of myoblasts over extracellular matrix.
S L Goodman, G Risse, K von der Mark.
J Cell Biol, 1989 Aug 01; 109(2). PMID: 2503526    Free PMC article.
Tumor-derived matrix metalloproteinase-13 (MMP-13) correlates with poor prognoses of invasive breast cancer.
Bin Zhang, Xuchen Cao, +10 authors, Xishan Hao.
BMC Cancer, 2008 Apr 01; 8. PMID: 18373849    Free PMC article.
Inhibition of cell adhesion by anti-adhesive molecules.
R Chiquet-Ehrismann.
Curr Opin Cell Biol, 1995 Oct 01; 7(5). PMID: 8573347
Review.
Structure and function of laminin: anatomy of a multidomain glycoprotein.
K Beck, I Hunter, J Engel.
FASEB J, 1990 Feb 01; 4(2). PMID: 2404817
Highly Cited. Review.
Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution.
Susann Schenk, Edith Hintermann, +4 authors, Vito Quaranta.
J Cell Biol, 2003 Apr 16; 161(1). PMID: 12695504    Free PMC article.
SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression.
Zhihu Ding, Chang-Jiun Wu, +25 authors, Ronald A DePinho.
Nature, 2011 Feb 04; 470(7333). PMID: 21289624    Free PMC article.
Highly Cited.
Ectopic production of MDA-7/IL-24 inhibits invasion and migration of human lung cancer cells.
Rajagopal Ramesh, Isao Ito, +3 authors, Sunil Chada.
Mol Ther, 2004 Apr 20; 9(4). PMID: 15093181
Cell migration: a physically integrated molecular process.
D A Lauffenburger, A F Horwitz.
Cell, 1996 Feb 09; 84(3). PMID: 8608589
Highly Cited. Review.
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists.
Da Wei Huang, Brad T Sherman, Richard A Lempicki.
Nucleic Acids Res, 2008 Nov 27; 37(1). PMID: 19033363    Free PMC article.
Highly Cited.
Laminin cleavage by activated human neutrophils yields proteolytic fragments with selective migratory properties.
R Steadman, M H Irwin, +3 authors, D R Abrahamson.
J Leukoc Biol, 1993 Apr 01; 53(4). PMID: 8482915
Laminin, a multidomain protein. The A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains.
M Sasaki, H K Kleinman, +2 authors, Y Yamada.
J Biol Chem, 1988 Nov 15; 263(32). PMID: 3182802
Highly Cited.
Laminin gamma2 mediates Wnt5a-induced invasion of gastric cancer cells.
Hideki Yamamoto, Yasuhiko Kitadai, +4 authors, Akira Kikuchi.
Gastroenterology, 2009 Jul 08; 137(1). PMID: 19582886
The coiled-coil structure potential of the laminin LCC domain is very fragmented and does not differentiate between natural and non-detected isoforms.
Tahl Zimmerman, Francisco J Blanco.
J Biomol Struct Dyn, 2007 Jan 09; 24(4). PMID: 17206855
The laminin B2 chain has a multidomain structure homologous to the B1 chain.
M Sasaki, Y Yamada.
J Biol Chem, 1987 Dec 15; 262(35). PMID: 3680290
Highly Cited.
Microarray and proteomic analysis of breast cancer cell and osteoblast co-cultures: role of osteoblast matrix metalloproteinase (MMP)-13 in bone metastasis.
Charlotte Morrison, Stephanie Mancini, +3 authors, Christopher Overall.
J Biol Chem, 2011 Jul 26; 286(39). PMID: 21784845    Free PMC article.
Broad coverage identification of multiple proteolytic cleavage site sequences in complex high molecular weight proteins using quantitative proteomics as a complement to edman sequencing.
Alain Doucet, Christopher M Overall.
Mol Cell Proteomics, 2010 Sep 30; 10(5). PMID: 20876890    Free PMC article.
The multicompartmental p32/gClqR as a new target for antibody-based tumor targeting strategies.
David Sánchez-Martín, Angel M Cuesta, +2 authors, Luis Alvarez-Vallina.
J Biol Chem, 2010 Dec 16; 286(7). PMID: 21156793    Free PMC article.
Linear models and empirical bayes methods for assessing differential expression in microarray experiments.
Gordon K Smyth.
Stat Appl Genet Mol Biol, 2006 May 02; 3. PMID: 16646809
Highly Cited.
A novel cell binding site in the coiled-coil domain of laminin involved in capillary morphogenesis.
Laura Sanz, Laura García-Bermejo, +5 authors, Luis Alvarez-Vallina.
EMBO J, 2003 Mar 28; 22(7). PMID: 12660158    Free PMC article.
Spindlin1, a novel nuclear protein with a role in the transformation of NIH3T3 cells.
Yanhong Gao, Wen Yue, +7 authors, Xuetao Pei.
Biochem Biophys Res Commun, 2005 Aug 16; 335(2). PMID: 16098913
A simplified laminin nomenclature.
Monique Aumailley, Leena Bruckner-Tuderman, +29 authors, Peter D Yurchenco.
Matrix Biol, 2005 Jun 28; 24(5). PMID: 15979864
Highly Cited. Review.
Gelatinase-mediated migration and invasion of cancer cells.
Mikael Björklund, Erkki Koivunen.
Biochim Biophys Acta, 2005 May 24; 1755(1). PMID: 15907591
Highly Cited. Review.
A peptide derived from laminin-γ3 reversibly impairs spermatogenesis in rats.
Linlin Su, Dolores D Mruk, +2 authors, C Yan Cheng.
Nat Commun, 2012 Nov 15; 3. PMID: 23149730    Free PMC article.
Generation and characterization of monospecific and bispecific hexavalent trimerbodies.
Ana Blanco-Toribio, Noelia Sainz-Pastor, +9 authors, Luis Álvarez-Vallina.
MAbs, 2012 Dec 12; 5(1). PMID: 23221741    Free PMC article.
Laminin 332 processing impacts cellular behavior.
Patricia Rousselle, Konrad Beck.
Cell Adh Migr, 2012 Dec 25; 7(1). PMID: 23263634    Free PMC article.
Review.
High EMT Signature Score of Invasive Non-Small Cell Lung Cancer (NSCLC) Cells Correlates with NFκB Driven Colony-Stimulating Factor 2 (CSF2/GM-CSF) Secretion by Neighboring Stromal Fibroblasts.
Albin Rudisch, Matthew Richard Dewhurst, +8 authors, Wolfgang Sommergruber.
PLoS One, 2015 Apr 29; 10(4). PMID: 25919140    Free PMC article.
Slc15a1 is involved in the transport of synthetic F5-peptide into the seminiferous epithelium in adult rat testes.
Linlin Su, Yufei Zhang, +3 authors, Dahai Hu.
Sci Rep, 2015 Nov 06; 5. PMID: 26537751    Free PMC article.
EventPointer: an effective identification of alternative splicing events using junction arrays.
Juan P Romero, Ander Muniategui, +4 authors, Angel Rubio.
BMC Genomics, 2016 Jun 19; 17. PMID: 27315794    Free PMC article.
Identification and quantification of sites of nitration and oxidation in the key matrix protein laminin and the structural consequences of these modifications.
Lasse G Lorentzen, Christine Y Chuang, Adelina Rogowska-Wrzesinska, Michael J Davies.
Redox Biol, 2019 Jun 04; 24. PMID: 31154162    Free PMC article.