Pericyte Biology - Novel Concepts

171 Pages·2018·5.188 MB·English

by  Alexander Birbrair

Advances in Experimental Medicine and Biology 1109
Alexander Birbrair E ditor
Pericyte
Biology
- Novel
Concepts
Advances in Experimental Medicine
and Biology
Volume 1109
Editorial Board:
IRUN R. COHEN, The Weizmann Institute of Science, Rehovot, Israel
ABEL LAJTHA, N.S. Kline Institute for Psychiatric Research, 
Orangeburg, NY, USA
JOHN D. LAMBRIS, University of Pennsylvania, Philadelphia, PA, USA
RODOLFO PAOLETTI, University of Milan, Milan, Italy
NIMA REZAEI,  Tehran University of Medical Sciences, Children’s Medical
Center Hospital, Tehran, Iran
More information about this series at http://www.springer.com/series/5584
Alexander Birbrair
Editor
Pericyte Biology - Novel
Concepts
Editor
Alexander Birbrair
Department of Radiology
Columbia University Medical Center
New York, NY, USA
Department of Pathology
Federal University of Minas Gerais
Belo Horizonte, MG, Brazil
ISSN 0065-2598 ISSN 2214-8019 (electronic)
Advances in Experimental Medicine and Biology
ISBN 978-3-030-02600-4 ISBN 978-3-030-02601-1 (eBook)
https://doi.org/10.1007/978-3-030-02601-1
Library of Congress Control Number: 2018964083
© Springer Nature Switzerland AG 2018
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microfilms or in any other physical way, and transmission or information
storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology
now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication
does not imply, even in the absence of a specific statement, that such names are exempt from the relevant
protective laws and regulations and therefore free for general use.
The publisher, the authors, and the editors are safe to assume that the advice and information in this book
are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the
editors give a warranty, express or implied, with respect to the material contained herein or for any errors
or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims
in published maps and institutional affiliations.
This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Preface
This book’s initial title was Pericyte Biology: Development, Homeostasis and
Disease. However, due to the current great interest in this topic, we were able to
assemble more chapters than would fit in one book, covering pericyte biology under
distinct circumstances. Therefore, the book was subdivided into three volumes enti-
tled Pericyte Biology - Novel Concepts, Pericyte Biology in Different Organs, and
Pericyte Biology in Disease.
This book, Pericyte Biology - Novel Concepts, presents contributions by expert
researchers and clinicians in the multidisciplinary areas of medical and biological
research. The chapters provide timely, detailed overviews of recent advances in the
field. This book describes the major contributions of pericytes to different organs’
biology in physiological and pathological conditions. Further insights into the biol-
ogy of pericytes will have important implications for our understanding of organ
development, homeostasis, and disease. The authors focus on the modern method-
ologies and the leading-edge concepts in the field of cell biology. In recent years,
remarkable progress has been made in the identification and characterization of
pericytes in several tissues using state-of-the-art techniques. These advantages facil-
itated the identification of pericyte subpopulations and definition of the molecular
basis of the role of pericytes within different organs. Thus, the present book is an
attempt to describe the most recent developments in the area of pericyte behavior,
which is one of the emergent hot topics in the field of molecular and cellular biology
today. Here, we present a selected collection of detailed chapters on what we know
so far about the pericytes in various tissues and under distinct pathophysiological
conditions. Ten chapters written by experts in the field summarize the present
knowledge about the physiological and pathophysiological roles of pericytes.
William B. Stallcup from Sanford Burnham Prebys Medical Discovery Institute
discusses the role of NG2 proteoglycan in pericyte biology. Bruno Péault and col-
leagues from the University of California describe the osteogenic potential of peri-
cytes and their use for therapeutic bone repair. Nabila Bahrami and Sarah J. Childs
from the University of Calgary compile our understanding of pericyte biology in
zebrafish. Paula Dore-Duffy and Nilufer Esen from Wayne State University update
us with the latest approaches for pericyte isolation, characterization, and cultivation.
v
vi Preface
Cristina L. Esteves and F. Xavier Donadeu from the University of Edinburgh
summarize the current knowledge on the properties of pericytes from domestic ani-
mals, and outline their potential use in clinical veterinary medicine. Kiminori Sato
from Kurume University School of Medicine addresses the importance of pericytes
in the human vocal fold mucosa. Theodor Burdyga and Lyudmyla Borysova from
the University of Liverpool focus on Ca2+ signaling in pericytes. Sharon Gerecht
and colleagues from Johns Hopkins University introduce our current knowledge
about pericytes derived from human pluripotent stem cells. Betül Çelebi-Saltik from
Hacettepe University discusses the possible use of pericytes in tissue engineering.
Finally, Abderahim Gaceb and Gesine Paul from Lund University give an overview
of pericyte secretome.
It is hoped that the articles published in this book will become a source of reference
and inspiration for future research ideas. I would like to express my deep gratitude
to my wife, Veranika Ushakova, and to Mr. Murugesan Tamilsevan from Springer,
who helped at every step of the execution of this project. This book is dedicated to
the memory of my grandfather, Pavel Sobolevsky z”l, PhD, a renowned mathemati-
cian, who passed away during the creation of this piece.
My grandfather, Pavel Sobolevsky z”l, PhD (March 26, 1930–August 16, 2018)
Belo Horizonte, Brazil Alexander Birbrair
Contents
1 Pericyte Biology: Development, Homeostasis, and Disease . . . . . . . . . . 1
Alexander Birbrair
2 The NG2 Proteoglycan in Pericyte Biology . . . . . . . . . . . . . . . . . . . . . . 5
William B. Stallcup
3 Pericytes for Therapeutic Bone Repair . . . . . . . . . . . . . . . . . . . . . . . . . . 21
Carolyn A. Meyers, Joan Casamitjana, Leslie Chang, Lei Zhang,
Aaron W. James, and Bruno Péault
4 Pericyte Biology in Zebrafish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
Nabila Bahrami and Sarah J. Childs
5 The Microvascular Pericyte: Approaches to Isolation,
Characterization, and Cultivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
Paula Dore-Duffy and Nilufer Esen
6 Pericytes in Veterinary Species: Prospective Isolation,
Characterization and Tissue Regeneration Potential . . . . . . . . . . . . . . 67
Cristina L. Esteves and F. Xavier Donadeu
7 Pericytes in the Human Vocal Fold Mucosa . . . . . . . . . . . . . . . . . . . . . . 79
Kiminori Sato
8 Ca2+ Signalling in Pericytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
Theodor Burdyga and Lyudmyla Borysova
9 Pericytes Derived from Human Pluripotent Stem Cells . . . . . . . . . . . . 111
John Jamieson, Bria Macklin, and Sharon Gerecht
10 Pericytes in Tissue Engineering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
Betül Çelebi-Saltik
11 Pericyte Secretome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139
Abderahim Gaceb and Gesine Paul
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165
vii
Contributors
Nabila Bahrami Department of Biochemistry and Molecular Biology, Alberta
Children’s Hospital Research Institute, University of Calgary, Calgary, AB, Canada
Alexander  Birbrair Department of Radiology, Columbia University Medical
Center, New York, NY, USA
Department of Pathology, Federal University of Minas Gerais, Belo Horizonte, MG,
Brazil
Lyudmyla Borysova Department of Pharmacology, University of Oxford, Oxford,
UK
Theodor Burdyga Department of Cellular and Molecular Physiology, Institute of
Translational Medicine, University of Liverpool, Liverpool, UK
Joan Casamitjana MRC Center for Regenerative Medicine, University of Edinburgh,
Edinburgh, UK
Betül Çelebi-Saltik Department of Stem Cell Sciences, Hacettepe University Graduate
School of Health Sciences, Ankara, Turkey
Center for Stem Cell Research and Development, Hacettepe University, Ankara,
Turkey
Leslie Chang Department of Pathology, Johns Hopkins University, Baltimore, MD,
USA
Sarah J. Childs Department of Biochemistry and Molecular Biology, Alberta
Children’s Hospital Research Institute, University of Calgary, Calgary, AB, Canada
Paula Dore-Duffy Department of Neurology, School of Medicine, Wayne State
University, Detroit, MI, USA
Nilufer Esen Department of Neurology, School of Medicine, Wayne State University,
Detroit, MI, USA
ix
x Contributors
Cristina  L.  Esteves Division of Developmental Biology, The Roslin Institute,
University of Edinburgh, Edinburgh, UK
Abderahim Gaceb Translational Neurology Group, Department of Clinical Sciences
and Wallenberg Center for Molecular Medicine, Department of Neurology, Lund
University, Lund, Sweden
Sharon Gerecht Department of Chemical and Biomolecular Engineering, Institute
for NanoBioTechnology, and the Physical Sciences-Oncology Center, Johns Hopkins
University, Baltimore, MD, USA
Aaron W. James Department of Pathology, Johns Hopkins University, Baltimore,
MD, USA
Orthopaedic Hospital Research Center, University of California, Los Angeles, CA,
USA
John Jamieson Department of Chemical and Biomolecular Engineering, Institute
for NanoBioTechnology, and the Physical Sciences-Oncology Center, Johns Hopkins
University, Baltimore, MD, USA
Bria Macklin Department of Chemical and Biomolecular Engineering, Institute
for NanoBioTechnology, and the Physical Sciences-Oncology Center, Johns Hopkins
University, Baltimore, MD, USA
Carolyn A. Meyers Department of Pathology, Johns Hopkins University, Baltimore,
MD, USA
Gesine Paul Translational Neurology Group, Department of Clinical Sciences and
Wallenberg Center for Molecular Medicine, Department of Neurology, Lund
University, Lund, Sweden
Skåne University Hospital, Lund, Sweden
Bruno Péault MRC Center for Regenerative Medicine, University of Edinburgh,
Edinburgh, UK
Orthopaedic Hospital Research Center, University of California, Los Angeles, CA,
USA
Kiminori Sato Department of Otolaryngology-Head and Neck Surgery, Kurume
University School of Medicine, Kurume, Japan
William B. Stallcup Tumor Microenvironment and Cancer Immunology Program,
Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, USA
F. Xavier Donadeu Division of Developmental Biology, The Roslin Institute,
University of Edinburgh, Edinburgh, UK
Euan MacDonald Centre for Motor Neurone Disease Research, University of
Edinburgh, Edinburgh, UK
Lei Zhang Department of Pathology, Johns Hopkins University, Baltimore, MD,
USA
Chapter 1
Pericyte Biology: Development,
Homeostasis, and Disease
Alexander Birbrair
In the nineteenth century, a French researcher, Charles-Marie Benjamin Rouget,
revealed a population of contractile cells associated with small blood vessels, which
were initially named after him as the Rouget cells [14]. In the twentieth century, a
German scientist, Karl Wilhelm Zimmermann, called these cells “pericytes” due to
their anatomical position located in a perivascular position [21]. The word pericyte
was derived from “peri” meaning “around” and “cyte” from the word “kytos” (cell),
illustrating a cell encircling a blood vessel [16]. Until now, pericytes are still identi-
fied partially based on their specific anatomical location and morphology. Pericytes
are present in all vascularized tissues, surrounding blood vessel walls [12]. They
encircle endothelial cells and communicate with them along the length of the blood
vessels by paracrine signaling and physical contacts [11]. Previously, the accurate
distinction of pericytes from other perivascular cells was difficult, as electron and
light microscopy were the sole available techniques capable to image these cells,
limiting the information acquired from those works. This resulted in the misleading
assumption that pericytes are merely inert supporting cells, limited exclusively to
the physiological function of vascular stability. In the last 10 years, the combination
of fluorescent and confocal microscopy with genetic state-of-art techniques, such as
fate lineage tracing, enabled remarkable progress in the discovery of multiple novel
essential functions for pericytes in health and disease, before unexpected [7].
Recently, the rapidly expanding understanding of the pathophysiological roles of
pericytes drew the attention of several research groups. Now, we know, for instance,
that pericytes may play immune functions [2]: attract innate leukocytes to exit via
sprouting blood vessels [19], regulate lymphocyte activation [15, 20], and contrib-
ute to the clearance of toxic by-products, having direct phagocytic activity [9].
Pericytes also may behave as stem cells [6], forming other cell populations, as well
A. Birbrair (*)
Department of Radiology, Columbia University Medical Center, New York, NY, USA
Department of Pathology, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
e-mail: [email protected]
© Springer Nature Switzerland AG 2018 1
A. Birbrair (ed.), Pericyte Biology - Novel Concepts, Advances in Experimental
Medicine and Biology 1109, https://doi.org/10.1007/978-3-030-02601-1_1