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Neutrophil Methods and Protocols 1st Edition Mark T.
Quinn Digital Instant Download
Author(s): Mark T. Quinn, Frank R. DeLeo (eds.)
ISBN(s): 9781627038447, 1627038442
Edition: 1
File Details: PDF, 6.95 MB
Year: 2014
Language: english

Neutrophil
Methods
andProtocols
MarkT. Quinn
Frank R.DeLeo Editors
SecondEdition
Methods in
Molecular Biology 1124

ME T H O D S I N MO L E C U L A R BI O LO G Y
Series Editor
John M. Walker
School of Life Sciences
University of Hertfordshire
Hatfield, Hertfordshire, AL10 9AB, UK
For further volumes:
http://www.springer.com/series/7651

Neutrophil Methods
and Protocols
Second Edition
Edited by
MarkT. Quinn
DepartmentofMicrobiologyandImmunology,MontanaStateUniversity,Bozeman,MT,USA
Frank R. DeLeo
Laboratory of Human Bacterial Pathogenesis, Rocky Mountain Laboratories,
NationalInstituteofAllergyandInfectiousDiseases,NationalInstitutesofHealth,Hamilton,MT,USA

ISSN 1064-3745 ISSN 1940-6029 (electronic)
ISBN 978-1-62703-844-7 ISBN 978-1-62703-845-4 (eBook)
DOI 10.1007
/978-1-62703-845-4
Springer New York Heidelberg Dordrecht London
Library of Congress Control Number: 2014930433
© Springer Science+Business Media, LLC 2014
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is
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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
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While the advice and information in this book are believed to be true and accurate at the date of publication, neither
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made. The publisher makes no warranty, express or implied, with respect to the material contained herein.
Printed on acid-free paper
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Springer is part of Springer Science+Business Media (www.springer.com)
Editors
Mark T. Quinn
Department of Microbiology and Immunology
Montana State University
Bozeman, MT, USA
Frank R. DeLeo
Laboratory of Human Bacterial Pathogenesis
Rocky Mountain Laboratories
National Institute of Allergy and Infectious
Diseases
National Institutes of Health
Hamilton, MT, USA

v
This volume is dedicated to Dr. Gary M. Bokoch (1954–2010) in recognition of his exten-
sive contributions to neutrophil biology and GTPase signaling. Gary was a good friend and
coeditor of the first edition of this volume. This volume is also dedicated to our families,
who are quite patient with all of the time we spend studying neutrophils.
Dedication

vii
Neutrophils [also known as polymorphonuclear leukocytes (PMNs) or granulocytes] are
the most abundant white cell in humans. Granulocytes and/or granulocyte precursors nor-
mally comprise ~60 % of the nucleated cells in bone marrow and blood. Mature neutrophils
have a typical circulating half-life of 6–8 h in the blood and then migrate through tissues
for ~2–3 days. Their relatively short life-span is devoted largely to surveillance for invading
microorganisms. During infection, the neutrophil life-span is extended, granulopoiesis
increases, and large numbers of neutrophils are rapidly recruited to the site(s) of infection.
Following recognition (binding) and phagocytosis of microorganisms, neutrophils utilize
an extraordinary array of oxygen-dependent and oxygen-independent microbicidal weap-
ons to destroy infectious agents. Oxygen-dependent mechanisms involve the production of
reactive oxygen species (ROS), while oxygen-independent mechanisms include degranula-
tion and release of lytic enzymes and bactericidal peptides. Inasmuch as these processes are
highly effective at killing most ingested microbes, neutrophils serve as the primary cellular
defense against infection.
The aim of Neutrophils: Methods and Protocols, Second Edition is to provide (1) a set of
protocols to assess most basic neutrophil functions, (2) protocols for investigating special-
ized areas in neutrophil research, and (3) step-by-step diagnostic assays for common neu-
trophil disorders. A wide variety of methods have been developed to assess neutrophil
function, and these methods have been instrumental in advancing our understanding of
the role of neutrophils in host defense and inflammatory disease. For those researchers and
clinicians interested in the study of neutrophils, the availability of a comprehensive source
of protocols describing the most modern methodological advances in neutrophil biology
is invaluable, as many publications do not provide information on the finer details critical
to success of a given method. As such, we have compiled a series of protocols written by
leading researchers in the field that provide detailed guidelines for establishing and per-
forming the most common neutrophil function assays. Hints of the best way to perform
these methods as well as guidance in detecting associated problems are included, so novice
investigators will also be able to effectively utilize these assays. While the volume provides
current protocols for evaluation of most basic neutrophil functions and certain specialized
functions, a section is dedicated to diagnostic assays for common neutrophil disorders.
Thus, this volume is designed for the basic researcher involved in the study of neutrophil
function and clinical investigators interested in medical aspects of neutrophil function in
health and disease.
In the second edition of Neutrophils: Methods and Protocols all of the chapters have
been updated, including many new approaches. In addition, the Second Edition contains
a number of new chapters that were not included in the First Edition. Part I is an over-
view of neutrophils and their role in host defense and inflammation. Part II describes the
most commonly used methods to isolate neutrophils from humans and other animal spe-
cies and procedures for subcellular fractionation of human neutrophils. This section also
contains a chapter that details collection and analysis of in vivo-transmigrated neutrophils.
Preface

viii
Part III encompasses protocols addressing neutrophil biochemistry, electrophysiology,
signal transduction, and apoptosis. New chapters covering neutrophil microinjection and
generation of mature neutrophils from induced pluripotent stem cells are now included.
Part IV details methods for investigating adhesion and chemotaxis, with new chapters on
evaluation of neutrophil migration through extracellular matrix and characterization of
outside-in signaling via integrins. Part V provides protocols for assessing neutrophil
phagocytosis and bactericidal activity, including new chapters that describe how to mea-
sure phagocytosis by flow cytometry and analyze formation and function of extracellular
traps. Part VI provides an extensive set of assays for evaluating NADPH oxidase priming
and activation, production of reactive oxygen species, and new chapters describing analy-
sis of p47phox
phosphorylation and flavocytochrome b conformational changes during
neutrophil activation. Part VII includes protocols to measure gene expression in neutro-
phils and a new chapter on high-purity neutrophil isolation from saliva for transcriptome
analysis. Finally, Part VIII provides assays for diagnosis of the most common neutrophil
disorders, including an updated section on assays for myeloperoxidase and myeloperoxi-
dase deficiency. In addition to the step-by-step protocols, the Notes section of each
chapter provides an outstanding depot of useful and interesting information not typically
published in the Methods sections of standard journal articles.
We thank John M. Walker, Series Editor, and Humana Press for the opportunity to
assemble an outstanding collection of articles and for help with the publication of the vol-
ume. We also thank the Montana State University COBRE Center for Zoonotic and
Emerging Infectious Diseases (NIH P20 GM103500) and the Intramural Research
Program of the NIH, National Institutes of Allergy and Infectious Diseases, for sponsoring
this volume. Finally, we thank the authors for taking time to write outstanding chapters.
Bozeman, MT, USA Mark T. Quinn
Hamilton, MT, USA Frank R. DeLeo
Preface

ix
Contents
Preface.................................................................................................................... vii
Contributors.................................................................................................................... xiii
PART I NEUTROPHILS: AN OVERVIEW
1 The Role of Neutrophils in the Immune System: An Overview......................... 3
Harry L. Malech, Frank R. DeLeo, and Mark T. Quinn
PART II NEUTROPHIL ISOLATION AND SUBCELLULAR FRACTIONATION
2 Isolation of Human Neutrophils from Venous Blood........................................ 13
William M. Nauseef
3 Neutrophil Isolation from Nonhuman Species.................................................. 19
Daniel W. Siemsen, Natalia Malachowa, Igor A. Schepetkin,
Adeline R. Whitney, Liliya N. Kirpotina, Benfang Lei, Frank
R. DeLeo, and Mark T. Quinn
4 Collection of In Vivo Transmigrated Neutrophils from Human Skin................. 39
Karin Christenson, Lena Björkman, Lisa Davidsson,
Anna Karlsson, Per Follin, Claes Dahlgren, and Johan Bylund
5 Subcellular Fractionation of Human Neutrophils
and Analysis of Subcellular Markers.................................................................. 53
Stine Novrup Clemmensen, Lene Udby, and Niels Borregaard
PART III BIOCHEMISTRY, BIOLOGY AND SIGNAL TRANSDUCTION
OF NEUTROPHILS
6 Rho Family and Rap GTPase Activation Assays................................................. 79
Richard T. Jennings and Ulla G. Knaus
7 Measurement of Phospholipid Metabolism in Intact Neutrophils...................... 89
Susan Sergeant and Linda C. McPhail
8 Optical Methods for the Measurement and Manipulation
of Cytosolic Calcium Signals in Neutrophils ..................................................... 107
Maurice B. Hallett, Maha Al-Jumaa, and Sharon Dewitt
9 Analysis of Electrophysiological Properties and Responses of Neutrophils......... 121
Deri Morgan and Thomas E. DeCoursey
10 Assessment of Neutrophil Apoptosis................................................................. 159
David A. Dorward, Adriano G. Rossi, Ian Dransfield,
and Christopher D. Lucas

x
11 Microinjection Methods for Neutrophils .......................................................... 181
Iraj Laffafian, Kimberly J. Lewis, K.Benjamin Masterman,
and Maurice B. Hallett
12 Generation of Functionally Mature Neutrophils from Induced
Pluripotent Stem Cells...................................................................................... 189
Colin L. Sweeney, Randall K. Merling, Uimook Choi,
Debra Long Priel, Douglas B. Kuhns, Hongmei Wang,
and Harry L. Malech
PART IV NEUTROPHIL ADHESION AND CHEMOTAXIS
13 Neutrophil Migration Through Extracellular Matrix......................................... 209
Richard T. Jennings and Ulla G. Knaus
14 Spinning Disk Confocal Imaging of Neutrophil Migration in Zebrafish ............ 219
Pui-ying Lam, Robert S. Fischer, William D. Shin, Clare M. Waterman,
and Anna Huttenlocher
15 Detection of Bidirectional Signaling During Integrin Activation
and Neutrophil Adhesion................................................................................. 235
Stuart M. Altman, Neha Dixit, and Scott I. Simon
PART V NEUTROPHIL PHAGOCYTOSIS AND BACTERICIDAL ACTIVITY
16 Immunofluorescence and Confocal Microscopy of Neutrophils......................... 251
Lee-Ann H. Allen
17 Expression of Genetically Encoded Fluorescent Probes
to Monitor Phospholipid Dynamics in Live Neutrophils................................... 269
Benjamin E. Steinberg, Marco A.O. Magalhaes, and Sergio Grinstein
18 Quantitative Assessment of Neutrophil Phagocytosis
Using Flow Cytometry..................................................................................... 279
Pontus Nordenfelt
19 Analysis of Neutrophil Bactericidal Activity....................................................... 291
Heather A. Parker, Nicholas J. Magon, Jessie N. Green,
Mark B. Hampton, and Christine C. Winterbourn
20 Induction and Quantification of Neutrophil Extracellular Traps........................ 307
Alejandro Sanchez Gonzalez, Bart W. Bardoel,
Christopher J. Harbort, and Arturo Zychlinsky
PART VI NADPH OXIDASE AND PRODUCTION
OF REACTIVE OXYGEN SPECIES
21 Measurement of Respiratory Burst Products, Released
or Retained, During Activation of Professional Phagocytes ............................... 321
Johan Bylund, Halla Björnsdottir, Martina Sundqvist,
Anna Karlsson, and Claes Dahlgren
22 Cell-Free NADPH Oxidase Activation Assays: “In Vitro Veritas”...................... 339
Edgar Pick
Contents

xi
23 Assessment of Priming of the Human Neutrophil Respiratory Burst ................. 405
Margarita Hurtado-Nedelec, Karama Makni-Maalej,
Marie-Anne Gougerot-Pocidalo, Pham My-Chan Dang,
and Jamel El-Benna
24 Affinity Purification and Reconstitution of Human Phagocyte
Flavocytochrome b for Detection of Conformational Dynamics
in the Membrane.............................................................................................. 413
Marcia Riesselman and Algirdas J. Jesaitis
25 Evaluation of p47phox Phosphorylation in Human Neutrophils
Using Phospho-Specific Antibodies.................................................................. 427
Sahra Amel Belambri, Pham My-Chan Dang, and Jamel El-Benna
PART VII ANALYSIS OF NEUTROPHIL GENE EXPRESSION
AND TRANSCRIPTION FACTORS
26 Genome-Scale Transcript Analyses with Human Neutrophils............................ 437
Scott D. Kobayashi, Daniel E. Sturdevant, and Frank R. DeLeo
27 Fast and Accurate Quantitative Analysis of Cytokine
Gene Expression in Human Neutrophils........................................................... 451
Nicola Tamassia, Marco A. Cassatella, and Flavia Bazzoni
28 High-Purity Neutrophil Isolation from Human Peripheral Blood
and Saliva for Transcriptome Analysis................................................................ 469
Flavia S. Lakschevitz and Michael Glogauer
29 Detection of Intact Transcription Factors in Human Neutrophils...................... 485
Patrick P. McDonald and Richard D. Ye
PART VIII NEUTROPHIL DEFECTS AND DIAGNOSIS
30 Disorders of Neutrophil Function: An Overview............................................... 501
Mary C. Dinauer
31 Diagnostic Assays for Chronic Granulomatous Disease
and Other Neutrophil Disorders....................................................................... 517
Houda Zghal Elloumi and Steven M. Holland
32 Diagnostic Assays for Myeloperoxidase and Myeloperoxidase Deficiency........... 537
William M. Nauseef
Index ............................................................................................................................... 547
Contents

xiii
MAHA AL-JUMAA • Neutrophil Signalling Group, School of Medicine, Cardiff University,
Cardiff, UK
LEE-ANN H. ALLEN • Inflammation Program and the Departments of Medicine
and Microbiology, University of Iowa and the VA Medical Center, Iowa City, IA, USA
STUART M. ALTMAN • Department of Biomedical Engineering, University of California,
Davis, CA, USA
BART W. BARDOEL • Department of Cellular Microbiology, Max Planck Institute for
Infection Biology, Berlin, Germany
FLAVIA BAZZONI • Section of General Pathology, Department of Pathology and Diagnostic,
University of Verona, Verona, Italy
SAHRA AMEL BELAMBRI • Département de Biologie, Faculté des Sciences, Université Ferhat
Abbas, Sétif, Algeria
LENA BJÖRKMAN • The Phagocyte Research Group, Department of Rheumatology
and Inflammation Research, University of Gothenburg, Gothenburg, Sweden
HALLA BJÖRNSDOTTIR • The Phagocyte Research Group, Department of Rheumatology
NIELS BORREGAARD • The Granulocyte Research Laboratory, Department of Hematology,
Rigshospitalet, Copenhagen University, Copenhagen, Denmark
JOHAN BYLUND • The Phagocyte Research Group, Department of Rheumatology
MARCO A. CASSATELLA • Section of General Pathology, Department of Pathology
and Diagnostic, University of Verona, Verona, Italy
UIMOOK CHOI • Laboratory of Host Defenses, National Institute of Allergy and Infectious
Diseases, National Institutes of Health, Bethesda, MD, USA
KARIN CHRISTENSON • Department of Rheumatology and Inflammation Research,
University of Gothenburg, Gothenburg, Sweden
STINE NOVRUP CLEMMENSEN • The Granulocyte Research Laboratory, Department of
Hematology, Rigshospitalet, Copenhagen University, Copenhagen, Denmark
CLAES DAHLGREN • The Phagocyte Research Group, Department of Rheumatology
PHAM MY-CHAN DANG • Faculté de Medecine, Centre de Recherche Biomédicale Bichat
Beaujon, INSERM U773, Paris, France
LISA DAVIDSSON • The Phagocyte Research Group, Department of Rheumatology
THOMAS E. DECOURSEY • Department of Molecular Biophysics and Physiology,
Rush University Medical Center, Chicago, IL, USA
FRANK R. DELEO • Laboratory of Human Bacterial Pathogenesis, Rocky Mountain
Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes
of Health, Hamilton, MT, USA
Contributors

xiv
SHARON DEWITT • Neutrophil Signalling Group, School of Medicine, Cardiff University,
Cardiff, UK
MARY C. DINAUER • Departments of Pediatrics (Hematology/Oncology) and Pathology &
Immunology, Washington University School of Medicine, St. Louis Children’s Hospital,
St. Louis, MO, USA
NEHA DIXIT • Department of Biomedical Engineering, University of California, Davis,
CA, USA
DAVID A. DORWARD • MRC Centre for Inflammation Research, Queen’s Medical Research
Institute, University of Edinburgh, Edinburgh, UK
IAN DRANSFIELD • MRC Centre for Inflammation Research, Queen’s Medical Research
JAMEL EL-BENNA • Faculté de Medecine, Centre de Recherche Biomédicale Bichat Beaujon,
INSERM U773, Paris, France
HOUDA ZGHAL ELLOUMI • Laboratory of Clinical Infectious Diseases, National Institute of
Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA
ROBERT S. FISCHER • Cell Biology and Physiology Center, National Heart, Lung, and Blood
Institute, National Institutes of Health, Bethesda, MD, USA
PER FOLLIN • Department of Communicable Disease Control and Prevention,
Västra Götaland Region, Gothenburg, Sweden
MICHAEL GLOGAUER • Department of Periodontology and Matrix Dynamics Group,
Faculty of Dentistry, University of Toronto, Toronto, ON, Canada
ALEJANDRO SANCHEZ GONZALEZ • Department of Cellular Microbiology, Max Planck
Institute for Infection Biology, Berlin, Germany
MARIE-ANNE GOUGEROT-POCIDALO • Centre de Recherche Biomédicale Bichat Beaujon,
JESSIE N. GREEN • Free Radical Research Group, Department of Pathology, Christchurch
School of Medicine, Christchurch, New Zealand
SERGIO GRINSTEIN • Cell Biology Programme, Hospital for Sick Children, Toronto,
ON, Canada
MAURICE B. HALLETT • Neutrophil Signalling Group, School of Medicine, Cardiff University,
Cardiff, UK
MARK B. HAMPTON • Free Radical Research Group, Department of Pathology, Christchurch
School of Medicine, Christchurch, New Zealand
CHRISTOPHER J. HARBORT • Department of Cellular Microbiology, Max Planck Institute
for Infection Biology, Berlin, Germany
STEVEN M. HOLLAND • Laboratory of Clinical Infectious Diseases, National Institute of
Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA
MARGARITA HURTADO-NEDELEC • Centre de Recherche Biomédicale Bichat Beaujon,
ANNA HUTTENLOCHER • Departments of Pediatrics and Pharmacology, University of
Wisconsin Medical School, Madison, WI, USA
RICHARD T. JENNINGS • Conway Institute, University College Dublin, Dublin, Ireland
ALGIRDAS J. JESAITIS • Department of Microbiology, Montana State University, Bozeman,
MT, USA
ANNA KARLSSON • The Phagocyte Research Group, Department of Rheumatology
LILIYA N. KIRPOTINA • Department of Immunology and Infectious Diseases, Montana State
University, Bozeman, MT, USA
Contributors

xv
ULLA G. KNAUS • Conway Institute, University College Dublin, Dublin, Ireland
SCOTT D. KOBAYASHI • Department of Microbiology, Molecular Biology, and Biochemistry,
University of Idaho, Moscow, ID, USA
DOUGLAS B. KUHNS • Neutrophil Monitoring Lab, Applied/Developmental Research
Directorate, Frederick National Laboratory on Cancer Research, Frederick, MD, USA
IRAJ LAFFAFIAN • Neutrophil Signalling Group, School of Medicine, Cardiff University,
Cardiff, UK
FLAVIA S. LAKSCHEVITZ • Matrix Dynamics Group, Faculty of Dentistry, University of
Toronto, Toronto, ON, Canada
PUI-YING LAM • Program in Cellular and Molecular Biology, University of Wisconsin-Madison,
Madison, WI, USA
BENFANG LEI • Department of Immunology and Infectious Diseases, Montana State University,
Bozeman, MT, USA
KIMBERLY J. LEWIS • Neutrophil Signalling Group, School of Medicine, Cardiff University,
Cardiff, UK
CHRISTOPHER D. LUCAS • MRC Centre for Inflammation Research, Queen’s Medical
Research Institute, University of Edinburgh, Edinburgh, UK
MARCO A.O. MAGALHAES • Cell Biology Programme, Hospital for Sick Children, Toronto,
ON, Canada
NICHOLAS J. MAGON • Free Radical Research Group, Department of Pathology,
Christchurch School of Medicine, Christchurch, New Zealand
KARAMA MAKNI-MAALEJ • Centre de Recherche Biomédicale Bichat Beaujon, INSERM U773,
Paris, France
NATALIA MALACHOWA • Laboratory of Human Bacterial Pathogenesis, Rocky Mountain
HARRY L. MALECH • Laboratory of Host Defenses, National Institute of Allergy
and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA
K. BENJAMIN MASTERMAN • Neutrophil Signalling Group, School of Medicine,
Cardiff University, Cardiff, UK
PATRICK P. MCDONALD • Department of Pharmacology, University of Illinois, Chicago,
IL, USA
LINDA C. MCPHAIL • Department of Biochemistry, Wake Forest University School of Medicine,
Winston-Salem, NC, USA
RANDALL K. MERLING • Laboratory of Host Defenses, National Institute of Allergy
DERI MORGAN • Department of Molecular Biophysics and Physiology, Rush University
Medical Center, Chicago, IL, USA
WILLIAM M. NAUSEEF • Inflammation Program and Department of Medicine, Roy J. and
Lucille A. Carver College of Medicine, University of Iowa, Coralville, IA, USA
PONTUS NORDENFELT • Department of Biological Chemistry and Molecular Pharmacology,
Harvard Medical School, Harvard University, Boston, MA, USA
HEATHER A. PARKER • Free Radical Research Group, Department of Pathology,
EDGAR PICK • The Julius Friedrich Cohnheim-Minerva Center for Phagocyte Research
and the Ela Kodesz Institute of Host Defense against Infectious Diseases, Sackler School of
Medicine, Tel Aviv University, Tel Aviv, Israel
Contributors

xvi
DEBRA LONG PRIEL • Neutrophil Monitoring Lab, Applied/Developmental Research
Directorate, Frederick National Laboratory on Cancer Research, Frederick, MD, USA
MARK T. QUINN • Department of Microbiology and Immunology, Montana State University,
Bozeman, MT, USA
MARCIA RIESSELMAN • Department of Microbiology, Montana State University, Bozeman,
MT, USA
ADRIANO G. ROSSI • MRC Centre for Inflammation Research, Queen’s Medical Research
IGOR A. SCHEPETKIN • Department of Immunology and Infectious Diseases, Montana State
SUSAN SERGEANT • Department of Biochemistry, Wake Forest University School of Medicine,
Winston-Salem, NC, USA
WILLIAM D. SHIN • Cell Biology and Physiology Center, National Heart, Lung, and Blood
Institute, National Institutes of Health, Bethesda, MD, USA
DANIEL W. SIEMSEN • Department of Immunology and Infectious Diseases, Montana State
SCOTT I. SIMON • Department of Biomedical Engineering, University of California, Davis,
CA, USA
BENJAMIN E. STEINBERG • Cell Biology Programme, Hospital for Sick Children, Toronto,
ON, Canada
DANIEL E. STURDEVANT • Genomics Unit, Rocky Mountain Laboratories, National Institute
of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT, USA
MARTINA SUNDQVIST • The Phagocyte Research Group, Department of Rheumatology
COLIN L. SWEENEY • Laboratory of Host Defenses, National Institute of Allergy
NICOLA TAMASSIA • Section of General Pathology, Department of Pathology and Diagnostic,
University of Verona, Verona, Italy
LENE UDBY • The Granulocyte Research Laboratory, Department of Hematology,
Rigshospitalet, Copenhagen University, Copenhagen, Denmark
HONGMEI WANG • Laboratory of Host Defenses, National Institute of Allergy and Infectious
Diseases, National Institutes of Health, Bethesda, MD, USA
CLARE M. WATERMAN • Cell Biology and Physiology Center, National Heart, Lung,
and Blood Institute, National Institutes of Health, Bethesda, MD, USA
ADELINE R. WHITNEY • Laboratory of Human Bacterial Pathogenesis, Rocky Mountain
CHRISTINE C. WINTERBOURN • Free Radical Research Group, Department of Pathology,
RICHARD D. YE • Department of Pharmacology, University of Illinois, Chicago, IL, USA
ARTURO ZYCHLINSKY • Department of Cellular Microbiology, Max Planck Institute for
Infection Biology, Berlin, Germany
Contributors

Part I
Neutrophils: An Overview

3
Mark T. Quinn and Frank R. DeLeo (eds.), Neutrophil Methods and Protocols, Methods in Molecular Biology, vol. 1124,
DOI 10.1007/978-1-62703-845-4_1, © Springer Science+Business Media, LLC 2014
Chapter 1
The Role of Neutrophils in the Immune
System: An Overview
Harry L. Malech, Frank R. DeLeo, and Mark T. Quinn
Abstract
Neutrophils, also known as polymorphonuclear leukocytes (PMNs), have long been considered as the
short-lived, nonspecific white cells that form pus—and also happen to kill invading microbes. Indeed,
neutrophils were often neglected (and largely not considered) as immune cells. This historic view of
neutrophils has changed considerably over the past several decades, and we know now that, in addition to
playing the predominant role in the clearance of bacteria and fungi, they play a major role in shaping the
host response to infection and immune system homeostasis. The change in our view of the role of neutro-
phils in the immune system has been due in large part to the study of these cells in vitro. Such work has
been made possible by new and/or improved methods and approaches used to investigate neutrophils.
These methods are the focus of this volume.
Key words Polymorphonuclear leukocyte, Granulocyte, Neutrophil methods
1 Introduction
This valuable and unique book contains a compendium of methods
and reviews that does much more than allow one to study the biol-
ogy of neutrophils. What makes this collection of contributions so
special is that it highlights and facilitates using the neutrophil as a
simple, pure, single primary cell suspension model to study a
remarkable array of generalized cellular functions (priming, che-
motaxis and transmigration, adhesion, phagocytosis, degranula-
tion, oxygen radical production, apoptosis, extracellular trap
formation), biochemical pathways (GTPase activation, phospho-
lipid metabolism, calcium transients, ion channel regulation, phos-
phorylation events, adhesion molecule regulation), as well as
specialized functions and molecules important to host defense
against infection, the mediation and resolution of inflammation,
and cytokine/chemokine modulation of immunity (see Fig. 1).
Consideration of the array of chapter topics evokes some of the
past history of inquiry into how neutrophils function and how we

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The Project Gutenberg eBook of Ornithological
biography, Vol. 4 (of 5)

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Title: Ornithological biography, Vol. 4 (of 5)
An account of the habits of the birds of the United
States of America
Author: John James Audubon
Contributor: William MacGillivray
Release date: December 2, 2023 [eBook #72279]
Language: English
Original publication: Edinburgh: Adam & Charles Black, 1835
Credits: Melissa McDaniel, Thierry Alberto, Thierry, Scholar and
the Online Distributed Proofreading Team at
https://www.pgdp.net (This file was produced from
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*** START OF THE PROJECT GUTENBERG EBOOK
ORNITHOLOGICAL BIOGRAPHY, VOL. 4 (OF 5) ***

Transcriber’s Note:
Inconsistent hyphenation, capitalization, and spelling in the
original document have been preserved. Obvious typographical
errors have been corrected.
The following inconsistencies were noted and retained:
Lorimier’s Fork, Lorimie’s Fork and Larimie’s Fork may be
the same place.
Grand Mannan and Grand Manan may be the same place.
J. R. Poinsett and Joel Poinsett may be the same person.
Mr Abbot and Mr Abbott may be the same person.
The following are possible errors, but retained:
Arkansa River should possibly be Arkansas.
gambling should possibly be gambolling.
Download Volume 1 at
https://www.gutenberg.org/ebooks/56989.

ORNITHOLOGICAL BIOGRAPHY,
OR AN ACCOUNT OF THE HABITS OF THE
BIRDS OF THE UNITED STATES OF AMERICA,
ACCOMPANIED BY DESCRIPTIONS OF THE OBJECTS REPRESENTED IN
THE WORK ENTITLED
BIRDS OF AMERICA,
TOGETHER WITH AN ACCOUNT OF THE DIGESTIVE ORGANS OF MANY OF
THE SPECIES, ILLUSTRATED BY ENGRAVINGS ON WOOD.

BY JOHN JAMES AUDUBON, F.R.SS.L.&E.
FELLOW OF THE LINNEAN AND ZOOLOGICAL SOCIETIES OF LONDON; MEMBER OF THE LYCEUM
OF NEW YORK, OF THE NATURAL HISTORY SOCIETY OF PARIS, THE WERNERIAN NATURAL
HISTORY SOCIETY OF EDINBURGH; HONORARY MEMBER OF THE SOCIETY OF NATURAL HISTORY
OF MANCHESTER, AND OF THE SCOTTISH ACADEMY OF PAINTING, SCULPTURE, AND
ARCHITECTURE; MEMBER OF THE AMERICAN PHILOSOPHICAL SOCIETY, OF THE ACADEMY OF
NATURAL SCIENCES AT PHILADELPHIA, OF THE NATURAL HISTORY SOCIETIES OF BOSTON, OF
CHARLESTON IN SOUTH CAROLINA, THE QUEBEC LITERARY AND HISTORICAL SOCIETY, THE
ORNITHOLOGICAL SOCIETY OF LONDON, &C. &C.
VOL. IV.
EDINBURGH:
ADAM & CHARLES BLACK, EDINBURGH:
LONGMAN, ORME, BROWN, GREEN &
LONGMANS, LONDON; R. HAVELL, ENGRAVER,
77. OXFORD STREET, LONDON; ALEXANDER
HILL, EDINBURGH; AND GEORGE SMITH,
LIVERPOOL.

PRINTED BY NEILL AND CO., OLD FISHMARKET, EDINBURGH.

INTRODUCTION.
Three years have nearly elapsed since I had the pleasure of
presenting you with the third volume of my “Ornithological
Biography,” and about twelve since the first fasciculus of my
“Illustrations of the Birds of America” was submitted to your
inspection. This work, comprising four hundred and thirty-five plates,
and one thousand and sixty-five figures, was finished on the 20th of
June 1838, without the continuity of its execution having been
broken for a single day, and the numbers having been delivered with
exemplary regularity; for all which I am indebted to my friend and
Engraver, Mr Robert Havell. Once more surrounded by all the
members of my dear family, enjoying the countenance of numerous
friends who have never deserted me, and possessing a competent
share of all that can render life agreeable, I look up with gratitude to
the Supreme Being, and feel that I am happy.

The adventures and vicissitudes which have fallen to my lot, instead
of tending to diminish the fervid enthusiasm of my nature, have
imparted a toughness to my bodily constitution, naturally strong, and
to my mind, naturally buoyant, an elasticity, such as to assure me
that, though somewhat old, and considerably denuded in the frontal
region, I could yet perform on foot a journey of any length, were I
sure that I should thereby add materially to our knowledge of the
ever-interesting creatures which have for so long a time occupied my
thoughts by day, and filled my dreams with pleasant images. Nay,
Reader, had I a new lease of life presented to me, I should chuse for
it the very occupations in which I have been engaged.
And, Reader, the life which I have led has been in some respects a
singular one. Think of a person intent on such pursuits as mine have
been, aroused at early dawn from his rude couch on the alder-
fringed brook of some northern valley, or in the midst of some yet
unexplored forest of the west, or perhaps on the soft and warm
sands of the Florida shores, and listening to the pleasing melodies of
songsters innumerable, saluting the magnificent orb from whose
radiant influence the creatures of many worlds receive life and light.
Refreshed and reinvigorated by healthful rest, he starts upon his
feet, gathers up his store of curiosities, buckles on his knapsack,
shoulders his trusty firelock, says a kind word to his faithful dog, and
recommences his pursuit of zoological knowledge. Now the morning
is spent, and a squirrel or a trout afford him a repast. Should the day
be warm, he reposes for a time under the shade of some tree. The
woodland choristers again burst forth into song, and he starts anew,
to wander wherever his fancy may direct him, or the objects of his
search may lead him in pursuit. When evening approaches and the
birds are seen betaking themselves to their retreats, he looks for
some place of safety, erects his shed of green boughs, kindles his
fire, prepares his meal, and as the Widgeon or Blue-winged Teal, or
perhaps the breast of a Turkey, or a steak of venison, sends its

delicious perfumes abroad, he enters into his parchment-bound
journal the remarkable incidents and facts that have occurred in the
course of the day. Darkness has now drawn her sable curtain over
the scene, his repast is finished, and kneeling on the earth he raises
his soul to Heaven, grateful for the protection that has been granted
to him and the sense of the Divine presence in this solitary place.
Then wishing a cordial good night to all the dear friends at home,
the American Woodsman wraps himself up in his blanket, and
closing his eyes, soon falls into that comfortable sleep which never
fails him on such occasions.
Since I last parted from you, my exertions have been unremitted,
and my rambles extended as far as circumstances allowed, for I
have been ever anxious to render the fourth and concluding volume
of my Illustrations as worthy of your approbation as I could. Whether
I have added to our knowledge of the birds which constantly reside
within the limits of the United States and their Territories, or
periodically visit us from the South, it is yours to say. That I have left
undone much that might have been accomplished by an abler
student of Nature, is doubtless quite true; but that any would have
prosecuted the study of our numerous feathered denizens with more
good will or more sincere desire to obtain facts and rectify errors,
would, I think, be difficult to prove. If my “Birds of America,” and
“Ornithological Biography,” are looked upon by you as having
contributed in some degree to the improvement of our knowledge of
these my favourite objects of observation, and as likely to stimulate
other and perhaps more successful students to perfect it. I shall rest
satisfied with my labours.
Having hitherto given you some account of the occurrences that
have taken place during the time intervening between the
appearance of one volume and that of another, I again resume the
subject, hoping that what I have now to say may prove not less
interesting to a friend like you. When I last left Edinburgh, I

proceeded to London, full of the desire to revisit my native land
before concluding my work. It was my wish to cross the Continent of
America, gaze on the majestic wilds of the Rocky Mountains, wander
along the green valleys of the Oregon, and search the shores of the
Pacific Ocean and a portion of North California; but circumstances
denied me the pleasure anticipated. However, here we are on the
way to the metropolis of England; we have already passed through
Newcastle, York, Leeds, and Manchester, and are just about to alight
in the Main Street of Sheffield. The gentleman who meets me at the
coach door, is John Heppenstall, Esq., well known to me by
correspondence, but not personally until now. Arrived here according
to appointment, we shake hands, and in a few minutes are beneath
his most hospitable roof, and in the midst of his family and friends.
The expectations which we had formed, so far from being
disappointed, were more than gratified, for this sincere and
honourable man is distinguished, not less by liberality of sentiment
than by a generosity commensurate with the goodness of his heart.
In these respects every member of his family is a counterpart of
himself; and, such being our hosts, you may judge how agreeable to
us was our stay in Sheffield. It was while enjoying the hospitality of
this excellent friend, that we became acquainted with Ebenezer
Elliot, Esq. and subsequently with Jonathan Brammell, Esq. from
whom we have since received many acts of kindness. Stopping
afterwards at Derby, we saw our relations there, and on arriving in
London were kindly welcomed by my brother-in-law, Alexander
Gordon, Esq., and soon established ourselves in a house in
Wimpole Street.
I now again enjoyed the society of our numerous friends, and had
the pleasure of seeing my work proceed apace. One day Mr Robert
Havell informed me, that a gentleman, a Fellow of the Royal
Society, residing not far from us, in the same street, had subscribed
for the Birds of America. The gentleman called to see me; my wife

and myself, were introduced to his lady, and the several members of
his amiable family, and our intimacy and friendship have ever since
increased. This excellent friend of mine is a surgeon of the highest
merit. Long before I left England for America, he took charge of my
wife’s precarious health; and when we parted at the coach that took
my son, John Woodhouse, and myself, to Portsmouth, he promised
to watch over her. When I again reached my house in Wimpole
Street, after an absence of a year, he was the first friend to greet me
with a cordial welcome. Were I to mention the many occasions on
which he has aided me by his advice and superior knowledge of the
world, you would be pleased to find so much disinterestedness in
human nature. His professional aid too, valuable as it has proved to
us, and productive of much inconvenience to him, has been
rendered without reward, for I could never succeed in inducing him
to consider us his patients, although for upwards of two years he
never passed a day without seeing my wife. But why should I say
more? This fine specimen of human nature, eminent for every virtue,
this kind and generous friend, is Benjamin Phillips, Esq.
Having been long anxious to introduce into America several species
of European birds, which I thought might thrive with us, I purchased
about an hundred individuals of that delightful songster, the Sky
Lark, fifty Starlings, and several Jays and Wood Pigeons, intending
to set them loose in the Western States. Putting them in ample
cages, accompanied with a store of food for the voyage, I had them
sent on board in the London Docks; but on our reaching Portsmouth
by land, we heard that the weather had been very bad in the
Channel, and that our birds had suffered severely. The news, to my
vexation, proved true; many of the birds had died; and, although our
passage to New York was pleasant as well as speedy, very few were
landed, so that my hopes were entirely disappointed.
On the 1st of August 1836, we went on board the fine American
Packet Ship, the Gladiator, commanded by Thomas Britton, Esq.

and proceeded on our voyage, which proved agreeable. On arriving
at New York, we soon reached the house of my good friend and
brother-in-law Nicholas Berthoud, Esq. Leaving my son there, I
proceeded almost immediately to Boston, where, under the roof of
my generous friend Dr George C. Shattuck, I enjoyed life for a
while. My friend Dr George Parkman was absent, and I missed him
much. Here, through the kindness of Dr Shattuck, I procured two
subscribers, and formed acquaintance with Thomas M. Brewer,
Esq., from whom I have received many valuable services, which you
will find mentioned in the proper places. Pushing on to Salem I
formed some acquaintances there, and procured several
subscribers; then returned to Boston, and as fortune would have it,
heard of the arrival of Thomas Nuttall, Esq., the well-known
zoologist, botanist, and mineralogist, who had performed a journey
over the Rocky Mountains to the Pacific Ocean, accompanied by our
mutual friend John Kirk Townsend, Esq., M. D. Mr Nuttall
generously gave me of his ornithological treasures all that was new,
and inscribed in my journal the observations which he had made
respecting the habits and distribution of all the new and rare species
which were unknown to me. All this information you will find in the
different articles to which it refers, and you will allow that while it
proves his zeal for the furtherance of science, it manifests the
generosity of his noble nature.
Dr Townsend’s collection was at Philadelphia; my anxiety to
examine his specimens was extreme; and I therefore, bidding
farewell to my Boston friends, hurried off to New York, where, in a
week, I added eighteen names to my list of subscribers, in obtaining
which I was materially aided by my brother-in-law. Once more my
son and I reached Philadelphia, where at once we placed ourselves
under the roof of my ever staunch and true friend Richard Harlan,
Esq., M. D., with whom we remained several weeks. Soon after my
arrival, I called on my learned friend Dr Charles Pickering, formed

the desired acquaintance of an enthusiastic young ornithologist,
James Trudeau, Esq., and met my firm friend Edward Harris,
Esq. Having obtained access to the collection sent by Dr Townsend,
I turned over and over the new and rare species; but he was absent
at Fort Vancouver, on the shores of the Columbia River; Thomas
Nuttall had not yet come from Boston, and loud murmurs were
uttered by the soi-disant friends of science, who objected to my
seeing, much less portraying and describing those valuable relics of
birds, many of which had not yet been introduced into our Fauna.
The traveller’s appetite is much increased by the knowledge of the
distance which he has to tramp before he can obtain a meal; and
with me the desire of obtaining the specimens in question increased
in proportion to the difficulties that presented themselves. Having
ascertained the names of the persons best able or most willing to
assist me on this occasion, and aided by Thomas Nuttall, who had
now arrived, Drs Pickering, Harlan, S. G. Morton, Secretary to
the Academy of Natural Sciences, M’Murtrie, Trudeau, and above
all my friend Edward Harris, who offered to pay for them with the
view of presenting them to me, I at length succeeded. It was agreed
that I might purchase duplicates, provided the specific names agreed
upon by Mr Nuttall and myself were published in Dr Townsend’s
name. This latter part of the affair was perfectly congenial to my
feelings, as I have seldom cared much about priority in the naming of
species. I therefore paid for the skins which I received, and have
now published such as proved to be new, according to my promise.
But, let me assure you, Reader, that seldom, if ever in my life, have I
felt more disgusted with the conduct of any opponents of mine, than I
was with the unfriendly boasters of their zeal for the advancement of
ornithological science, who at the time existed in the fair city of
Philadelphia.
From Philadelphia I bent my course toward Baltimore, where I spent
a few days. Before leaving the former city, my good friend Edward

Harris had promised to join us at Charleston, for the purpose of
accompanying us along the western coast of the Floridas, and the
Gulf of Mexico, at least as far as Galveston Island in Texas. On
reaching the city of Washington, I presented myself to the
Honourable Levi Woodbury, Secretary of the Treasury of the
United States, a gentleman of learning, long friendly towards me,
who at once assured me that he would, if possible, grant me one of
our Revenue Cutters, for my intended voyage. The war, which was
at that time raging between the Seminole Indians and the citizens of
Florida tended strongly to frustrate my wishes, as every disposable
vessel of the class under the Secretary of the Treasury was engaged
on the coast of the Peninsula. I called on President Andrew
Jackson, from whom, since 1819, I have received peculiar facilities,
and who assured me of his wish to grant my request. My son and I
dined with him on that day sans façon, both of us in the undress best
suited to practical students of nature. And here I may inform you,
that I have seldom eaten of a better Wild Turkey than the one which
graced his table, and which had been procured not many miles
distant from our centre of political intercourse. I also had the
pleasure of seeing my excellent friend, Colonel J. J. Abert, of the U.
S. Topographical Department, the Honourable J. R. Poinsett, and
the Secretary of the Navy, to whom I then recommended several
American naturalists as worthy of being engaged on any naval
expedition of discovery.
We now proceeded towards Charleston in South Carolina, travelling
the latter part of the way on one of the most extraordinary rail-roads
in the world, and reached in safety the house of my worthy friend the
Reverend John Bachman, D.D. It was indeed a happy meeting!
Here I opened the box containing Dr Townsend’s precious series of
birds, and while waiting the arrival of Mr Harris, drew upwards of
seventy figures of the species which I had procured at Philadelphia,
assisted in the finishing of the plants, branches of trees, and flowers,

which accompany these figures, by my friend’s sister-in-law Miss M.
Martin, to whom I now again offer my most sincere thanks. While
here I received the agreeable intelligence of my having been elected
a Member of the Ornithological Society of London.
Edward Harris joined me, but the Revenue Cutter had not made
its appearance; and time becoming precious, on account of the
approach of spring, we bid adieu to all at Charleston, and pushed for
New Orleans, where, I was informed by Government letters, I should
meet with a vessel. On reaching Augusta in Georgia, I called on Dr
Wray, who promised to forward to me a number of plants for my
noble friend Lord Ravensworth, who has received them in good
order. After several days of severe travelling, we arrived at
Montgomery in Alabama, and meeting there with a steam-boat
bound to Mobile, secured our passage. Next day we arrived there,
and spent two days in examining the neighbourhood; after which we
proceeded to Pensacola, where I felt proud to find a harbour
commodious enough to contain a fleet sufficient to repel the attacks
of any naval force brought against the United States. Here I made
the long-sought-for acquaintance of Mr Innerarity, to whom I had
letters from my friend Alexander Gordon, Esq., and who
introduced us to all who were likely to forward our views. The next
morning he accompanied us on board the United States’ frigate, the
Constellation, and presented us to Commodore Dallas, to whom I
had letters of introduction from our government. This polite and
gallant officer received us all with great kindness, and, after reading
my letters, assured me that as soon as a cutter could be spared, it
should be at my service, and that the information would be
transmitted to me through the medium of the Collector of Customs at
Mobile or New Orleans. After searching the country around
Pensacola, we returned to Mobile, and proceeded to New Orleans in
a steamer, by way of the great lakes.

Having previously received the most pressing invitation from my
friend James Grimshaw, Esq., my son and I went at once to his
house, where we were treated with all the kindness to be expected
from a true English gentleman. I had the pleasure of renewing my
acquaintance with Ex-Governor Roman, and several members of his
most amiable family, among whom was Mr Zaringue. From that
gentleman I received much valuable information respecting some of
our birds, as well as from my long-known acquaintance, the great
sportsman Mr Louis Adam. Here also I for the last time met with
good M. Le Sueur, well known to the world of science as a zoologist
of great merit, and with whom I first became acquainted at
Philadelphia in 1824. He, alas! is now no more.
Having called on Mr Breedlove, Collector of Customs for New
Orleans, and presented to him my letters from the Honourable Levi
Woodbury, he at once assured me that the Revenue Cutter the
Campbell, would be at my disposal in a very few days. But the
service, or other circumstances, did not allow the arrival of that
vessel at New Orleans until late in March, and at a time when,
apprehensive that our intended voyage might be frustrated, we were
all “crest-fallen.” Time, however, passed on, and one morning I was
gladdened by being called upon by the Commander of the Campbell,
and still more upon recognising in him the Lieutenant and Pilot of the
Marion, or Lady of the Green Mantle, so frequently mentioned in the
former volumes of these Ornithological Biographs. I knew that
Napoleon Coste was a true sea-fowl. He assured me of the
excellence of his vessel, and gay and happy were we all when we
removed on board the tight little sea-boat, of scarcely more than
sixty tons burden. Proceeding down the Mississippi, we sailed
through its south-west Pass, where we were joined by a vessel of
eight tons, as a tender for our excursions along the shores. It was
commanded by Captain William Taylor, now, I believe, a

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