Patterns in expression of insulin-like growth factor-II and of proliferative activity in the normal human first and third trimester placenta demonstrated by non-isotopic in situ hybridization and immunohistochemical staining for MIB-1

doi:10.1016/S0143-4004(97)90086-2

Placenta

Volume 18, Issues 2–3, March–April 1997, Pages 145-154

https://doi.org/10.1016/S0143-4004(97)90086-2 Get rights and content

Abstract

The expression of insulin-like growth factor-11 (IGF-1I) in normal human first and third trimester placental tissue was investigated by non-isotopic in situ hybridization (ISH). This is the first ISH study on IGF-11 expression in placenta using an alkaline phosphatase-labelled probe. The expression was correlated with the proliferative activity of the cells using the proliferative marker MIB-1. In first trimester tissue, IGF-II was expressed in the cytotrophoblast, the extravillous trophoblast, the fetal endothelial cells and the mesenchymal fetal cells in the villi. In third trimester tissue, IGF-11 expression was found in the amnion, the extravillous trophoblast and the mesenchymal fetal cells especially in the endothelial cells and the outer contractile sheet in the stem villi. In areas with perivillous fibrin deposits, strong expression of IGF-11 was found in the cytotrophoblasts invading the fibrin. In first trimester tissue, the proliferative activity of the villous cytotrophoblast correlated well with the degree of IGF-II expression whereas in third trimester tissue, there was a discrepancy between MIB-1 positivity and the IGF-11 expression. Expression of IGF-II does not seem to be correlated exclusively to the mitogenic activity of cells.

References (47)

P. Bischof et al.
Expression of extracellular matrix-degrading metalloproteinases by cultured human cytotrophoblast cells: Effects of cell adhesion and immunopurification
American Journal of Obstetrics and Gynecogy
(1991)
T.N. Blankenship et al.
Identification of 72-kilodalton type IV collagenase at sites of trophoblastic invasion of macaque spiral arteries
Placenta,
(1994)
R.A. Brace
Progress toward understanding the regulation of amniotic fluid volume: water and solute fluxes in and through the fetal membranes
Placenta
(1995)
M.P. Czech
Signal transmission by the insulin-like growth factors
Cell
(1989)
T.M. DeChiara et al.
Parental Imprinting of the Mouse Insulin-like Growth Factor II Gene
Cell
(1991)
H. Fox et al.
Effect of hypoxia on trophoblast in organ culture: a morphologic and autoradiographic study
American Journal of Obstetrics and Gynaecology
(1970)
D.J. Hill et al.
Immunohistochemical localization of Insulin-like growth factors (IGFs) and IGF binding proteins-1, -2 and -3 in human placenta and fetal membranes
Placenta
(1993)
Y. Ichimiya et al.
Insulin-like growth factor II in the rat choroid plexus
Molecular Brain Research
(1988)
J.A. Irving et al.
Characteristics of trophoblast cells migrating from first trimester chorionic villus explants and propagated in culture
Placenta
(1995)
W. Kiess et al.
Biochemical evidence that the type II insulin-like growth factor receptor identical to the cation-independent mannose 6-phosphate receptor
Journal of Biological Chemistry
(1988)

H. Kiyama et al.

Recent progress in the use of the technique of non-radioactive in situ hybridization histochemistry: A new tool for molecular neurobiology

Neuroscience Research

(1990)

T.M. Mayhew et al.

Quantitative evidence for the spatial dispersal of trophoblast nuclei in human placental villi during gestation

Placenta

(1994)

L.A. Milio et al.

Binding of insulin-like growth factor I to human trophoblast cells during differentiation in vitro

Placenta

(1994)

Y. Oh et al.

Demonstration of receptors for insulin-like growth factor binding protein-3 on Hs578T human breast cancer cells

Biological Chemistry

(1993)

R.C.M. Simmen et al.

Insulin-like growth factors and blastocyst development

Theriogenology

(1993)

J.S. Sussenbach

The gene structure of the Insulin-like growth factor family

Progress in Growth Factor Research

(1989)

L. Vicovac et al.

Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro

Placenta

(1995)

A. Ward et al.

Repression of promoters for the mouse insulin-like growth factor II-encoding gene (Igf-2) by products of the Wilms' tumour suppressor gene wtl

Gene

(1995)

D.P. Barlow et al.

The mouse insulin-like growth factor type-2 receptor is imprinted and closely related to the Tme locus

Nature

(1991)

A.L. Brace et al.

Temporal changes in the expression of the insulin-like growth factor II gene associated with tissue maturation in the human fetus

Development

(1989)

T.M. DeChiara et al.

A growthdeficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting

Nature

(1990)

H. Emonard et al.

Type IV and interstitial collagenolytic activities in normal and malignant trophoblast cells are specifically regulated by the extracellular matrix

Invasion Metastasis

(1990)

H. Fox

The villous cytotrophoblast as an index of placental ischaemia

Journal of Obstetrics and Gynaecology of the British Commonmealth

(1964)

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Original articlePatterns in expression of insulin-like growth factor-II and of proliferative activity in the normal human first and third trimester placenta demonstrated by non-isotopic in situ hybridization and immunohistochemical staining for MIB-1

Abstract

American Journal of Obstetrics and Gynecogy

Placenta,

Placenta

Cell

Cell

American Journal of Obstetrics and Gynaecology

Placenta

Molecular Brain Research

Placenta

Journal of Biological Chemistry

Neuroscience Research

Placenta

Placenta

Biological Chemistry

Theriogenology

Progress in Growth Factor Research

Placenta

Gene

The mouse insulin-like growth factor type-2 receptor is imprinted and closely related to the Tme locus

Nature

Temporal changes in the expression of the insulin-like growth factor II gene associated with tissue maturation in the human fetus

Development

A growthdeficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting

Nature

Type IV and interstitial collagenolytic activities in normal and malignant trophoblast cells are specifically regulated by the extracellular matrix

Invasion Metastasis

The villous cytotrophoblast as an index of placental ischaemia

Journal of Obstetrics and Gynaecology of the British Commonmealth

Original article
Patterns in expression of insulin-like growth factor-II and of proliferative activity in the normal human first and third trimester placenta demonstrated by non-isotopic in situ hybridization and immunohistochemical staining for MIB-1