Laminin and heparan sulfate proteoglycan mediate epithelial cell polarization in organotypic cultures of embryonic lung cells: Evidence implicating involvement of the inner globular region of laminin β1 chain and the heparan sulfate groups of heparan sulfate proteoglycan

Lucia Schuger, Amy P Skubitz, Kevin Gilbride, Richard Mandel, Li He

Research output: Contribution to journalArticle

38 Citations (Scopus)

Abstract

The extracellular matrix and in particular the basement membrane (BM) play an important role in the induction of organotypic rearrangement of cells in culture. This process involves cell aggregation, sorting into epithelial and mesenchymal components, epithelial cell polarization, and lumen formation. In this study, a combination of laminin (LM) and heparan sulfate proteoglycan (HSPG), two major BM constituents, induced organotypic rearrangement of embryonic mouse lung cells, In the absence of LM/HSPG supplementation, the cells sorted into epithelial and mesenchymal compartments but epithelial cell polarization and lumen formation did not occur. Neither LM nor HSPG alone could trigger this process. Synthetic peptide F-9, representing an amino acid sequence from the inner globular region of the laminin β1 chain (RYVVLPRPVCFEKGMNYTVR) induced organotypic cell rearrangement when substituted for LM. Exogenous LM as well as peptide F-9 were localized at the epithelial-mesenchymal interface of organotypic cultures, where a BM-like structure is formed de novo. Organotypic cell rearrangement was blocked by heparin, heparan sulfate, or antibodies against peptide F-9. Binding assays indicated that peptide F-9 interacts with HSPG but not with LM or type IV collagen. Preincubation of embryonic lung cells with peptide F-9 resulted in a significant increase in cell attachment to HSPG but not to other major BM constituents. These findings suggest that the interaction between LM and BM HSPG is critical for the development of epithelial cell polarization and lumen formation. This interaction occurs at the epithelial-mesenchymal interface and is mediated by a site in the LM molecule represented by peptide F-9 and the-heparan sulfate groups of HSPG.

Original languageEnglish (US)
Pages (from-to)264-273
Number of pages10
JournalDevelopmental Biology
Volume179
Issue number1
DOIs
StatePublished - Oct 10 1996

Fingerprint

Heparan Sulfate Proteoglycans
Heparitin Sulfate
Laminin
Epithelial Cells
Lung
Basement Membrane
Cell Aggregation
Collagen Type IV
laminin 1
Extracellular Matrix
Heparin
peptide F
Amino Acid Sequence
Cell Culture Techniques
Antibodies

Cite this

@article{794dadddfc7f409a8c663f3a75cf21d2,
title = "Laminin and heparan sulfate proteoglycan mediate epithelial cell polarization in organotypic cultures of embryonic lung cells: Evidence implicating involvement of the inner globular region of laminin β1 chain and the heparan sulfate groups of heparan sulfate proteoglycan",
abstract = "The extracellular matrix and in particular the basement membrane (BM) play an important role in the induction of organotypic rearrangement of cells in culture. This process involves cell aggregation, sorting into epithelial and mesenchymal components, epithelial cell polarization, and lumen formation. In this study, a combination of laminin (LM) and heparan sulfate proteoglycan (HSPG), two major BM constituents, induced organotypic rearrangement of embryonic mouse lung cells, In the absence of LM/HSPG supplementation, the cells sorted into epithelial and mesenchymal compartments but epithelial cell polarization and lumen formation did not occur. Neither LM nor HSPG alone could trigger this process. Synthetic peptide F-9, representing an amino acid sequence from the inner globular region of the laminin β1 chain (RYVVLPRPVCFEKGMNYTVR) induced organotypic cell rearrangement when substituted for LM. Exogenous LM as well as peptide F-9 were localized at the epithelial-mesenchymal interface of organotypic cultures, where a BM-like structure is formed de novo. Organotypic cell rearrangement was blocked by heparin, heparan sulfate, or antibodies against peptide F-9. Binding assays indicated that peptide F-9 interacts with HSPG but not with LM or type IV collagen. Preincubation of embryonic lung cells with peptide F-9 resulted in a significant increase in cell attachment to HSPG but not to other major BM constituents. These findings suggest that the interaction between LM and BM HSPG is critical for the development of epithelial cell polarization and lumen formation. This interaction occurs at the epithelial-mesenchymal interface and is mediated by a site in the LM molecule represented by peptide F-9 and the-heparan sulfate groups of HSPG.",
author = "Lucia Schuger and Skubitz, {Amy P} and Kevin Gilbride and Richard Mandel and Li He",
year = "1996",
month = "10",
day = "10",
doi = "10.1006/dbio.1996.0256",
language = "English (US)",
volume = "179",
pages = "264--273",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "1",

}

TY - JOUR

T1 - Laminin and heparan sulfate proteoglycan mediate epithelial cell polarization in organotypic cultures of embryonic lung cells

T2 - Evidence implicating involvement of the inner globular region of laminin β1 chain and the heparan sulfate groups of heparan sulfate proteoglycan

AU - Schuger, Lucia

AU - Skubitz, Amy P

AU - Gilbride, Kevin

AU - Mandel, Richard

AU - He, Li

PY - 1996/10/10

Y1 - 1996/10/10

N2 - The extracellular matrix and in particular the basement membrane (BM) play an important role in the induction of organotypic rearrangement of cells in culture. This process involves cell aggregation, sorting into epithelial and mesenchymal components, epithelial cell polarization, and lumen formation. In this study, a combination of laminin (LM) and heparan sulfate proteoglycan (HSPG), two major BM constituents, induced organotypic rearrangement of embryonic mouse lung cells, In the absence of LM/HSPG supplementation, the cells sorted into epithelial and mesenchymal compartments but epithelial cell polarization and lumen formation did not occur. Neither LM nor HSPG alone could trigger this process. Synthetic peptide F-9, representing an amino acid sequence from the inner globular region of the laminin β1 chain (RYVVLPRPVCFEKGMNYTVR) induced organotypic cell rearrangement when substituted for LM. Exogenous LM as well as peptide F-9 were localized at the epithelial-mesenchymal interface of organotypic cultures, where a BM-like structure is formed de novo. Organotypic cell rearrangement was blocked by heparin, heparan sulfate, or antibodies against peptide F-9. Binding assays indicated that peptide F-9 interacts with HSPG but not with LM or type IV collagen. Preincubation of embryonic lung cells with peptide F-9 resulted in a significant increase in cell attachment to HSPG but not to other major BM constituents. These findings suggest that the interaction between LM and BM HSPG is critical for the development of epithelial cell polarization and lumen formation. This interaction occurs at the epithelial-mesenchymal interface and is mediated by a site in the LM molecule represented by peptide F-9 and the-heparan sulfate groups of HSPG.

AB - The extracellular matrix and in particular the basement membrane (BM) play an important role in the induction of organotypic rearrangement of cells in culture. This process involves cell aggregation, sorting into epithelial and mesenchymal components, epithelial cell polarization, and lumen formation. In this study, a combination of laminin (LM) and heparan sulfate proteoglycan (HSPG), two major BM constituents, induced organotypic rearrangement of embryonic mouse lung cells, In the absence of LM/HSPG supplementation, the cells sorted into epithelial and mesenchymal compartments but epithelial cell polarization and lumen formation did not occur. Neither LM nor HSPG alone could trigger this process. Synthetic peptide F-9, representing an amino acid sequence from the inner globular region of the laminin β1 chain (RYVVLPRPVCFEKGMNYTVR) induced organotypic cell rearrangement when substituted for LM. Exogenous LM as well as peptide F-9 were localized at the epithelial-mesenchymal interface of organotypic cultures, where a BM-like structure is formed de novo. Organotypic cell rearrangement was blocked by heparin, heparan sulfate, or antibodies against peptide F-9. Binding assays indicated that peptide F-9 interacts with HSPG but not with LM or type IV collagen. Preincubation of embryonic lung cells with peptide F-9 resulted in a significant increase in cell attachment to HSPG but not to other major BM constituents. These findings suggest that the interaction between LM and BM HSPG is critical for the development of epithelial cell polarization and lumen formation. This interaction occurs at the epithelial-mesenchymal interface and is mediated by a site in the LM molecule represented by peptide F-9 and the-heparan sulfate groups of HSPG.

UR - http://www.scopus.com/inward/record.url?scp=0030579162&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0030579162&partnerID=8YFLogxK

U2 - 10.1006/dbio.1996.0256

DO - 10.1006/dbio.1996.0256

M3 - Article

C2 - 8873769

AN - SCOPUS:0030579162

VL - 179

SP - 264

EP - 273

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 1

ER -