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PMID: 3942197 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Basement membrane as a spatial organizer of polarized epithelia. Exogenous basement membrane reorients pancreatic epithelial tumor cells in vitro.

The American journal of pathology ·Vol. 122 ·No. 1 ·1986-01-00 ·Pages 129-39

Ingber DE, Madri JA, Jamieson JD

Abstract

The authors have previously described a transplantable pancreatic acinar carcinoma that comprises cells which reorganize and display normal epithelial orientation only when in contact with basement membrane (BM) in vivo. In the present study, they investigated whether exogenous acellular BM or collagenous stroma (prepared from human amnion) was sufficient to reorient pancreatic acinar tumor cells in vitro. Mechanically dispersed tumor cells could not spontaneously attach to standard culture substrata; yet they adhered to exogenous intact BM or to dishes coated with purified laminin or Type IV collagen. Cell contact with amniotic BM resulted in tumor cell shape changes, assembly of intracellular actin into fibrous bundles, and restoration of normal epithelial cell-cell interactions. Computerized morphometry confirmed that tumor cells exhibited a normal polarized distribution of lipid droplets, nuclei, Golgi complexes, and zymogen granules (from base to apex) within 6 hours of culture on BM. Adhering zonules and microvilli were observed only along apical tumor cell surfaces, although full junctional complexes and distinct membrane domains did not reform. Similar attachment, cytoskeletal alterations, and reorientation occurred in the absence of protein synthesis (25 micrograms/ml cycloheximide). In contrast, tumor cells that were maintained on amniotic stroma remained round, displayed circumferential rings of actin, and appeared randomly oriented. Thus, BM may normally serve to integrate and maintain individual cells within a polarized epithelium.

MeSH Terms
Amnion Animals Basement Membrane/physiology Carcinoma/pathology,ultrastructure Cell Adhesion Cell Aggregation Cells, Cultured Cytoskeleton/ultrastructure Epithelium/pathology,ultrastructure Intercellular Junctions/ultrastructure Male Microscopy, Electron Microvilli/ultrastructure Pancreatic Neoplasms/pathology,ultrastructure Rats Rats, Inbred F344
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ingber D E
Madri J A
Jamieson J D
References (46)
46 references, click to expand
  1. Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: possible mechanism for basal lamina formation.
    Proc Natl Acad Sci U S A. 1979 Feb;76(2):786-90 PMID: 284399
  2. Nature of the collagenous protein in a tumor basement membrane.
    Eur J Biochem. 1978 Mar;84(1):43-52 PMID: 648517
  3. Intracellular transport and storage of secretory proteins in relation to cytodifferentiation in neoplastic pancreatic acinar cells.
    J Cell Biol. 1983 Apr;96(4):949-60 PMID: 6833397
  4. Structure and composition of early basement membranes: studies with early embryos and teratocarcinoma cells.
    Med Biol. 1983 Feb;61(1):1-30 PMID: 6341722
  5. Basement membrane polarizes lectin binding sites of Drosophila larval fat body cells.
    Nature. 1983 May 26;303(5915):340-2 PMID: 6406896
  6. Characterization of protease-resistant fragments of laminin mediating attachment and spreading of rat hepatocytes.
    J Biol Chem. 1983 Jul 25;258(14):8922-7 PMID: 6408095
  7. Role of laminin in epithelium formation by F9 aggregates.
    J Cell Biol. 1983 Jul;97(1):137-44 PMID: 6190817
  8. Capillary endothelial cell cultures: phenotypic modulation by matrix components.
    J Cell Biol. 1983 Jul;97(1):153-65 PMID: 6190818
  9. Connectin: cell surface protein that binds both laminin and actin.
    Proc Natl Acad Sci U S A. 1983 Oct;80(19):5927-30 PMID: 6310604
  10. Cultured endothelial cell monolayers that restrict the transendothelial passage of macromolecules and electrical current.
    J Cell Biol. 1984 Mar;98(3):1033-41 PMID: 6699080
  11. An acellular human amnionic membrane model for in vitro culture of type II pneumocytes: the role of the basement membrane in cell morphology and function.
    J Cell Physiol. 1984 Oct;121(1):215-25 PMID: 6548224
  12. Differentiation of pancreatic acinar carcinoma cells cultured on rat testicular seminiferous tubular basement membranes.
    Cancer Res. 1984 Nov;44(11):5361-8 PMID: 6488190
  13. Neoplastic disorganization of pancreatic epithelial cell-cell relations. Role of basement membrane.
    Am J Pathol. 1985 Nov;121(2):248-60 PMID: 4061565
  14. The Golgi apparatus in chick corneal epithelium: changes in intracellular position during development.
    J Cell Biol. 1970 Apr;45(1):34-42 PMID: 4195852
  15. Studies on dispersed pancreatic exocrine cells. I. Dissociation technique and morphologic characteristics of separated cells.
    J Cell Biol. 1974 Dec;63(3):1037-56 PMID: 4373477
  16. Fetal membrane collagens: identification of two new collagen alpha chains.
    Proc Natl Acad Sci U S A. 1976 Aug;73(8):2579-83 PMID: 1066666
  17. Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology.
    J Cell Biol. 1977 May;73(2):445-63 PMID: 858743
  18. Development of the embryonic mammalian pancreas: the relationship between morphogenesis and cytodifferentiation.
    Dev Biol. 1977 Dec;61(2):119-30 PMID: 563351
  19. Assembly of enveloped viruses in Madin-Darby canine kidney cells: polarized budding from single attached cells and from clusters of cells in suspension.
    J Cell Biol. 1983 Mar;96(3):866-74 PMID: 6300140
  20. Role of cell shape in growth control.
    Nature. 1978 Jun 1;273(5661):345-9 PMID: 661946
  21. Determination of cellular shape by the extracellular matrix and its correlation with the control of cellular growth.
    Cancer Res. 1978 Nov;38(11 Pt 2):4155-71 PMID: 359133
  22. Ca++-dependent disassembly and reassembly of occluding junctions in guinea pig pancreatic acinar cells. Effect of drugs.
    J Cell Biol. 1978 Oct;79(1):156-72 PMID: 701369
  23. Asymmetric budding of viruses in epithelial monlayers: a model system for study of epithelial polarity.
    Proc Natl Acad Sci U S A. 1978 Oct;75(10):5071-5 PMID: 283416
  24. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes.
    In Vitro. 1977 May;13(5):316-28 PMID: 559643
  25. Transplantable pancreatic carcinoma of the rat.
    Science. 1977 Oct 7;198(4312):78-80 PMID: 897688
  26. Basement membrane collagen requirements for attachment and growth of mammary epithelium.
    Exp Cell Res. 1979 Nov;124(1):181-90 PMID: 499382
  27. Fluorescent phallotoxin, a tool for the visualization of cellular actin.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4498-502 PMID: 291981
  28. Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):485-9 PMID: 6987652
  29. Silicone rubber substrata: a new wrinkle in the study of cell locomotion.
    Science. 1980 Apr 11;208(4440):177-9 PMID: 6987736
  30. Structural and functional membrane polarity in cultured monolayers of MDCK cells.
    J Membr Biol. 1980;52(2):147-59 PMID: 6245216
  31. Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney. an immunoferritin study of ultrathin frozen sections.
    J Cell Biol. 1980 Jun;85(3):597-616 PMID: 6993495
  32. Ultrastructural localization of fibronectin and laminin in the basement membranes of the murine kidney.
    J Cell Biol. 1980 Aug;86(2):682-7 PMID: 6995470
  33. Protein synthesis requires cell-surface contact while nuclear events respond to cell shape in anchorage-dependent fibroblasts.
    Cell. 1980 Sep;21(2):365-72 PMID: 6157481
  34. Apical membrane aminopeptidase appears at site of cell-cell contact in cultured kidney epithelial cells.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):4132-6 PMID: 6933462
  35. Isolation of a heparan sulfate-containing proteoglycan from basement membrane.
    Proc Natl Acad Sci U S A. 1980 Aug;77(8):4494-8 PMID: 6449008
  36. Conditioned medium from endothelial cell cultures can restore the normal phenotypic expression of vascular endothelium maintained in vitro in the absence of fibroblast growth factor.
    J Cell Physiol. 1980 May;103(2):333-47 PMID: 6969261
  37. The collagenous components of the subendothelium. Correlation of structure and function.
    Lab Invest. 1980 Oct;43(4):303-15 PMID: 7003251
  38. Effects of inhibition of basement membrane collagen deposition on rat mammary gland development.
    Dev Biol. 1980 Dec;80(2):253-6 PMID: 7450284
  39. New method for preparing large surfaces of intact human basement membrane for tumor invasion studies.
    Cancer Lett. 1980 Dec;11(2):141-52 PMID: 7459842
  40. Role of laminin in the attachment of PAM 212 (epithelial) cells to basement membrane collagen.
    Cell. 1980 Dec;22(3):719-26 PMID: 7460011
  41. Possible functions of mesenchyme cell-derived fibronectin during formation of basal lamina.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3711-5 PMID: 6943577
  42. Role of basal lamina in neoplastic disorganization of tissue architecture.
    Proc Natl Acad Sci U S A. 1981 Jun;78(6):3901-5 PMID: 7022458
  43. Influence of collagen gel on the orientation of epithelial cell polarity: follicle formation from isolated thyroid cells and from preformed monolayers.
    J Cell Biol. 1981 Oct;91(1):157-66 PMID: 7298715
  44. Response of basal epithelial cell surface and Cytoskeleton to solubilized extracellular matrix molecules.
    J Cell Biol. 1981 Oct;91(1):45-54 PMID: 7197682
  45. Comparison of secretory protein profiles in developing rat pancreatic rudiments and rat acinar tumor cells.
    J Cell Biol. 1982 Dec;95(3):742-6 PMID: 6185503
  46. Laminin--a glycoprotein from basement membranes.
    J Biol Chem. 1979 Oct 10;254(19):9933-7 PMID: 114518
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
1986-01-00
Pages
129-39
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1888129
Subset
IM
Grants
NIADDK NIH HHS · AM-17389 · United States
NIGMS NIH HHS · GM-07205 · United States
NHLBI NIH HHS · HL-28373 · United States
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