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PMID: 1849141 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

92-kD type IV collagenase mediates invasion of human cytotrophoblasts.

The Journal of cell biology ·Vol. 113 ·No. 2 ·1991-04-00 ·Pages 437-49

Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ

Abstract

The specialized interaction between embryonic and maternal tissues is unique to mammalian development. This interaction begins with invasion of the uterus by the first differentiated embryonic cells, the trophoblasts, and culminates in formation of the placenta. The transient tumor-like behavior of cytotrophoblasts, which peaks early in pregnancy, is developmentally regulated. Likewise, in culture only early-gestation human cytotrophoblasts invade a basement membrane-like substrate. These invasive cells synthesize both metalloproteinases and urokinase-type plasminogen activator. Metalloproteinase inhibitors and a function-perturbing antibody specific for the 92-kD type IV collagen-degrading metalloproteinase completely inhibited cytotrophoblast invasion, whereas inhibitors of the plasminogen activator system had only a partial (20-40%) inhibitory effect. We conclude that the 92-kD type IV collagenase is critical for cytotrophoblast invasion.

MeSH Terms
Antibody Specificity Basement Membrane/metabolism Cell Aggregation Cells, Cultured Embryonic and Fetal Development Female Humans Matrix Metalloproteinase 9 Microbial Collagenase/antagonists & inhibitors,immunology,metabolism Microscopy, Electron, Scanning Photomicrography Pregnancy Trophoblasts/metabolism,ultrastructure
Chemicals
Microbial Collagenase Matrix Metalloproteinase 9
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Librach C L
Department of Stomatology, University of California, San Francisco 94143.
Werb Z
Fitzgerald M L
Chiu K
Corwin N M
Esteves R A
Grobelny D
Galardy R
Damsky C H
Fisher S J
References (72)
72 references, click to expand
  1. Mouse L cells expressing human prourokinase-type plasminogen activator: effects on extracellular matrix degradation and invasion.
    J Cell Biol. 1989 Aug;109(2):915-25 PMID: 2503527
  2. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro.
    J Cell Biol. 1989 Aug;109(2):891-902 PMID: 2474556
  3. Limited cleavage of cellular fibronectin by plasminogen activator purified from transformed cells.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2776-80 PMID: 3033662
  4. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  5. Metalloproteinases and their inhibitors in matrix remodeling.
    Trends Genet. 1990 Apr;6(4):121-5 PMID: 2132731
  6. Selection of B16 melanoma cells with increased metastatic potential and low intercellular cohesion using Nuclepore filters.
    Invasion Metastasis. 1985;5(1):1-15 PMID: 3980159
  7. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts.
    Lab Invest. 1989 Jul;61(1):20-6 PMID: 2473276
  8. Expression of the c-fms proto-oncogene and of the cytokine, CSF-1, during mouse embryogenesis.
    Dev Biol. 1989 May;133(1):284-94 PMID: 2523324
  9. Plasminogen activators in tissue remodeling and invasion: mRNA localization in mouse ovaries and implanting embryos.
    J Cell Biol. 1989 Nov;109(5):2471-9 PMID: 2509486
  10. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells.
    J Exp Zool. 1989 Aug;251(2):167-85 PMID: 2549171
  11. Cleavage of type VII collagen by interstitial collagenase and type IV collagenase (gelatinase) derived from human skin.
    J Biol Chem. 1989 Mar 5;264(7):3822-6 PMID: 2537292
  12. In vivo invasion of modified chorioallantoic membrane by tumor cells: the role of cell surface-bound urokinase.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2437-45 PMID: 2848851
  13. Developmental expression of tissue inhibitor of metalloproteinase (TIMP) RNA.
    Development. 1989 Mar;105(3):575-83 PMID: 2693036
  14. Proteinases and extracellular matrix remodeling.
    Curr Opin Cell Biol. 1989 Oct;1(5):974-82 PMID: 2697298
  15. Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts.
    J Biol Chem. 1987 Aug 15;262(23):10903-6 PMID: 3301845
  16. Activation of pro-urokinase and plasminogen on human sarcoma cells: a proteolytic system with surface-bound reactants.
    J Cell Biol. 1989 May;108(5):1987-95 PMID: 2523891
  17. Characterization of gelatinase from pig polymorphonuclear leucocytes. A metalloproteinase resembling tumour type IV collagenase.
    Biochem J. 1989 Mar 1;258(2):463-72 PMID: 2539808
  18. Tissue cooperation in a proteolytic cascade activating human interstitial collagenase.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2632-6 PMID: 2468156
  19. Genes for extracellular-matrix-degrading metalloproteinases and their inhibitor, TIMP, are expressed during early mammalian development.
    Genes Dev. 1989 Jun;3(6):848-59 PMID: 2744464
  20. Transforming growth factor-beta induction of type-1 plasminogen activator inhibitor. Pericellular deposition and sensitivity to exogenous urokinase.
    J Biol Chem. 1987 Dec 25;262(36):17467-74 PMID: 3121597
  21. H-ras oncogene-transformed human bronchial epithelial cells (TBE-1) secrete a single metalloprotease capable of degrading basement membrane collagen.
    J Biol Chem. 1988 May 15;263(14):6579-87 PMID: 2834383
  22. The plasminogen system and cell surfaces: evidence for plasminogen and urokinase receptors on the same cell type.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2411-20 PMID: 3023400
  23. A metalloproteinase from human rheumatoid synovial fibroblasts that digests connective tissue matrix components. Purification and characterization.
    J Biol Chem. 1986 Oct 25;261(30):14245-55 PMID: 3095317
  24. Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells.
    Cancer Res. 1988 Jun 15;48(12):3307-12 PMID: 2836052
  25. Purification and characterization of an elastinolytic proteinase secreted by cercariae of Schistosoma mansoni.
    J Biol Chem. 1985 Mar 25;260(6):3703-7 PMID: 3882713
  26. Purification and characterization of a bone metalloproteinase that degrades gelatin and types IV and V collagen.
    Biochim Biophys Acta. 1985 Sep 20;831(1):49-58 PMID: 2994741
  27. Plasminogen activators, tissue degradation, and cancer.
    Adv Cancer Res. 1985;44:139-266 PMID: 2930999
  28. Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collagenase. Biosynthesis, isolation, characterization, and substrates.
    J Biol Chem. 1985 Oct 5;260(22):12367-76 PMID: 2995374
  29. Immunocytochemical localization of tissue kallikrein in brain ventricular epithelium and hypothalamic cell bodies.
    J Histochem Cytochem. 1985 Sep;33(9):951-3 PMID: 3894505
  30. Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro.
    Proc Natl Acad Sci U S A. 1986 Jun;83(12):4167-71 PMID: 2424019
  31. Secretion of metalloproteinases by stimulated capillary endothelial cells. II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors.
    J Biol Chem. 1986 Feb 25;261(6):2814-8 PMID: 3005266
  32. Inhibition of tumor-cell-mediated extracellular matrix destruction by a fibroblast proteinase inhibitor, protease nexin I.
    Proc Natl Acad Sci U S A. 1986 Feb;83(4):996-1000 PMID: 3513169
  33. Inhibition by human recombinant tissue inhibitor of metalloproteinases of human amnion invasion and lung colonization by murine B16-F10 melanoma cells.
    Cancer Res. 1988 Oct 1;48(19):5539-45 PMID: 3416307
  34. Biochemical interactions of tumor cells with the basement membrane.
    Annu Rev Biochem. 1986;55:1037-57 PMID: 3017189
  35. SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages.
    J Biol Chem. 1989 Oct 15;264(29):17213-21 PMID: 2551898
  36. Human placenta protein-tyrosine-phosphatase: amino acid sequence and relationship to a family of receptor-like proteins.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5252-6 PMID: 2546149
  37. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade.
    Cell. 1986 Nov 21;47(4):487-98 PMID: 3022933
  38. Type X collagen contains two cleavage sites for a vertebrate collagenase.
    J Biol Chem. 1986 Mar 25;261(9):4184-9 PMID: 3005323
  39. Synthetic substrates of vertebrate collagenase.
    Biochemistry. 1985 Nov 5;24(23):6730-4 PMID: 3002449
  40. The extracellular matrix of normal chick embryo fibroblasts: its effect on transformed chick fibroblasts and its proteolytic degradation by the transformants.
    J Cell Biol. 1985 Nov;101(5 Pt 1):1790-8 PMID: 2997235
  41. Cell-associated plasminogen activation: regulation and physiological functions.
    Annu Rev Cell Biol. 1988;4:93-126 PMID: 3143380
  42. Heterogeneous expression of keratin, involucrin, and extracellular matrix among subpopulations of a poorly differentiated human cervical carcinoma: possible relationships to patterns of invasion.
    Cancer Res. 1989 Jun 1;49(11):3007-14 PMID: 2470500
  43. Regulation of cell adhesion receptors by transforming growth factor-beta. Regulation of vitronectin receptor and LFA-1.
    J Biol Chem. 1989 Jan 5;264(1):389-92 PMID: 2462560
  44. Heterogeneous expression of cytokeratins in metastatic mammary adenocarcinoma cells in vitro and in vivo.
    Invasion Metastasis. 1987;7(6):367-83 PMID: 2449401
  45. A rapid in vitro assay for quantitating the invasive potential of tumor cells.
    Cancer Res. 1987 Jun 15;47(12):3239-45 PMID: 2438036
  46. Temporal expression and location of colony-stimulating factor 1 (CSF-1) and its receptor in the female reproductive tract are consistent with CSF-1-regulated placental development.
    Proc Natl Acad Sci U S A. 1989 Nov;86(22):8818-22 PMID: 2554332
  47. Use of inhibitory (anti-catalytic) antibodies to study extracellular proteolysis.
    Immunol Invest. 1989 Jan-May;18(1-4):211-24 PMID: 2543625
  48. Regulation of cell adhesion receptors by transforming growth factor-beta. Concomitant regulation of integrins that share a common beta 1 subunit.
    J Biol Chem. 1989 Jan 5;264(1):380-8 PMID: 2491849
  49. A new in vitro assay for quantitating tumor cell invasion.
    Invasion Metastasis. 1989;9(3):192-208 PMID: 2722434
  50. Intermediate trophoblast: a distinctive form of trophoblast with specific morphological, biochemical and functional features.
    Placenta. 1984 Jul-Aug;5(4):349-69 PMID: 6209706
  51. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae.
    Endocrinology. 1986 Apr;118(4):1567-82 PMID: 3512258
  52. Expression of rat transforming growth factor alpha mRNA during development occurs predominantly in the maternal decidua.
    Mol Cell Biol. 1987 Jul;7(7):2335-43 PMID: 3475565
  53. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix.
    J Biol Chem. 1986 Mar 25;261(9):4337-45 PMID: 3456347
  54. A simple quantitative assay for studying the invasive potential of high and low human metastatic variants.
    Cancer Lett. 1987 Dec;38(1-2):137-47 PMID: 3690504
  55. Invasion of reconstituted basement membrane matrix by metastatic human tumor cells.
    Cancer Res. 1986 Apr;46(4 Pt 2):1980-9 PMID: 3948175
  56. Mr 92,000 gelatinase release correlates with the metastatic phenotype in transformed rat embryo cells.
    Cancer Res. 1990 Jul 1;50(13):3872-7 PMID: 2162246
  57. Differential susceptibility of type X collagen to cleavage by two mammalian interstitial collagenases and 72-kDa type IV collagenase.
    J Biol Chem. 1990 Aug 15;265(23):13521-7 PMID: 2166034
  58. Human trophoblast-extracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity.
    Proc Natl Acad Sci U S A. 1990 Apr;87(8):3057-61 PMID: 2326266
  59. Inner cell allocation in the mouse morula: the role of oriented division during fourth cleavage.
    Dev Biol. 1990 Jan;137(1):13-25 PMID: 2295360
  60. Aggregation of dispersed human cytotrophoblastic cells: lessons relevant to the morphogenesis of the placenta.
    Dev Biol. 1990 Jan;137(1):100-8 PMID: 2295358
  61. Degradation of extracellular matrix by mouse trophoblast outgrowths: a model for implantation.
    J Cell Biol. 1983 Apr;96(4):1108-16 PMID: 6339525
  62. Effect of natural protease inhibitors and a chemoattractant on tumor cell invasion in vitro.
    J Natl Cancer Inst. 1982 Nov;69(5):1049-54 PMID: 6752521
  63. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates.
    Anal Biochem. 1980 Feb;102(1):196-202 PMID: 7188842
  64. Biochemical actions of glucocorticoids on macrophages in culture. Specific inhibition of elastase, collagenase, and plasminogen activator secretion and effects on other metabolic functions.
    J Exp Med. 1978 Jun 1;147(6):1695-1712 PMID: 210248
  65. Endogenous activation of latent collagenase by rheumatoid synovial cells. Evidence for a role of plasminogen activator.
    N Engl J Med. 1977 May 5;296(18):1017-23 PMID: 66627
  66. Phorbol ester-induced morphological changes in transformed chick fibroblasts: evidence for direct catalytic involvement of plasminogen activator.
    Cell. 1979 May;17(1):131-41 PMID: 222474
  67. Preferential digestion of basement membrane collagen by an enzyme derived from a metastatic murine tumor.
    Proc Natl Acad Sci U S A. 1979 May;76(5):2268-72 PMID: 221920
  68. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  69. Implantation. The role of proteinases, and blockage of implantation by proteinase inhibitors.
    Adv Anat Embryol Cell Biol. 1977;53(5):3-123 PMID: 602861
  70. Cytology of human early implantation.
    Res Reprod. 1976 Sep;8(5):1-2 PMID: 1028113
  71. Plasminogen activator in early embryogenesis: enzyme production by trophoblast and parietal endoderm.
    Cell. 1976 Oct;9(2):231-40 PMID: 975245
  72. Cleavage of Type II and III collagens with mammalian collagenase: site of cleavage and primary structure at the NH2-terminal portion of the smaller fragment released from both collagens.
    Biochemistry. 1976 Feb 24;15(4):787-92 PMID: 174719
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1991-04-00
Pages
437-49
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2288933
Subset
IM
Grants
NICHD NIH HHS · HD 22518 · United States
NICHD NIH HHS · HD 23539 · United States
NICHD NIH HHS · P01 HD 2418 · United States
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