HISTOLOGY AND HISTOPATHOLOGY

From Cell Biology to Tissue Engineering

 

Changes in vascular extracellular matrix composition during decidual spiral arteriole remodeling in early human pregnancy

Samantha D. Smith1,2, Ruhul H. Choudhury1,2, Patricia Matos1,2, James A. Horn1,2, Stephen J. Lye3, Caroline E. Dunk3, John D. Aplin1,2, Rebecca L. Jones1,2 and Lynda K Harris1,2,4

1Maternal and Fetal Health Research Centre (MFHRC), Institute of Human Development, University of Manchester, 2Maternal and Fetal Health Research Centre (MFHRC), St. Mary's Hospital, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Science Centre, Manchester, UK, 3Departments of Physiology and Obstetrics and Gynecology, Women’s and Infant’s Health, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada and 4Manchester Pharmacy School, Stopford Building, Manchester, UK

Offprint requests to: Lynda K. Harris, Maternal and Fetal Health Research Centre, 5th Floor (Research), St. Mary’s Hospital, Oxford Road, Manchester, M13 9WL, UK. e-mail: lynda.k.harris@manchester.ac.uk


Summary. Uterine spiral arteriole (SA) remodeling in early pregnancy involves a coordinated series of events including decidual immune cell recruitment, vascular cell disruption and loss, and colonization by placental-derived extravillous trophoblast (EVT). During this process, decidual SA are converted from narrow, muscular vessels into dilated channels lacking vasomotor control. We hypothesized that this extensive alteration in SA architecture must require significant reorganization and/or breakdown of the vascular extracellular matrix (ECM). First trimester decidua basalis (30 specimens) was immunostained to identify spiral arterioles undergoing trophoblast-independent and -dependent phases of remodeling. Serial sections were then immunostained for a panel of ECM markers, to examine changes in vascular ECM during the remodeling process. The initial stages of SA remodeling were characterized by loss of laminin, elastin, fibrillin, collagen types III, IV and VI from the basement membrane, vascular media and/or adventitia, and surrounding decidual stromal cells. Loss of ECM correlated with disruption and disorganization of vascular smooth muscle cells, and the majority of changes occurred prior to extensive colonization of the vessel wall by EVT. The final stages of SA remodeling, characterized by the arrival of EVT, were associated with the increased mural deposition of fibronectin and fibrinoid. This study provides the first detailed analysis of the spatial and temporal loss of ECM from the walls of remodeling decidual SA in early pregnancy. Histol Histopathol 31, 557-571 (2016)

Key words: Extracellular matrix, Extravillous trophoblast, Placenta, Spiral arteriole, Vascular remodeling

DOI: 10.14670/HH-11-696