Gwendalyn J. Randolph

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Gwendalyn J. Randolph
GwenRandolphHeadshot.jpg
Born
Hart, Texas, U.S.
Alma mater Temple University
State University of New York, Stony Brook
Known forDendritic cell differentiation and trafficking, immune cell and lipoprotein trafficking in inflammatory bowel disease and atherosclerosis
AwardsAmerican Heart Association Established Investigator Award, Pioneer Award for High Risk High Reward Initiative Programs NIH Director's Office, NIH MERIT Award, Special Recognition Award in Atherosclerosis American Heart Association
Scientific career
FieldsImmunology, vascular biology
Institutions Washington University in St. Louis, Mount Sinai School of Medicine

Gwendalyn J. Randolph is an American immunologist, the Emil R. Unanue Distinguished Professor in the Department of Immunology and Pathology at Washington University School of Medicine where she is currently co-director of the Immunology Graduate Program. During her postdoctoral work, Randolph characterized monocyte differentiation to dendritic cells and macrophages and made advances in our understanding of dendritic cell trafficking and the fate of monocytes recruited to sites of inflammation. Her lab has contributed to the Immunological Genome Project by characterizing macrophage gene expression. Her work now focuses on the immunological mechanisms driving atherosclerosis and inflammatory bowel disease (IBD) by exploring lymphatic function and lipoprotein trafficking.

Contents

Early life and education

Randolph, born Gwendalyn Wilson, was born in the small farming town of Hart, Texas. [1] She grew up helping her parents on their maize and cotton farm by tending to weeds and helping with harvests. [1] At school at Hart High School, she showed an early passion for design and textiles, [2] winning awards and funding to travel to New York and Los Angeles for her sewing achievements. [1] She accepted a sports scholarship to play basketball at Wayland Baptist University in Plainview, Texas in 1987, and majored in biology. [2]

In 1989, she married Keith Randolph; they moved to the east coast where she continued her studies at Temple University in Philadelphia, Pennsylvania. [2] She graduated with a Bachelors of Science in biological sciences in 1991, . [1] She received her PhD in Immunology and Pathology in 1995 from the State University of New York, Stony Brook. [3] working under the mentorship of Martha B. Furie studying themoocyte migration. [4]

Randolph stayed in New York for postdoctoral training at The Rockefeller University and Weill Medical College of Cornell University in the departments of Cellular Immunology and Pathology. [1] She worked under the mentorship of Bill Muller, vascular biologist, and Ralph Steinman studying dendritic cell maturation and migration. [1]

Dendritic cell maturation and migration

Randolph's postdoctoral work, in collaboration with Steinman and Muller, investigated the differentiation of dendritic cells and their migration to lymph nodes from the periphery. [5] She developed an in vitro model to assess monocyte differentiation into dendritic cells (DCs) or macrophages. [6] They found that exposure of monocytes to endothelial cells was critical to DC differentiation and that exposure to phagocytic particles caused cells that had previously reverse-transmigrated to fully displayed a DC-like phenotype in terms of intracellular and extracellular markers as well as a highly ramified phenotype. [6] Randolph also showed that monocytes could also differentiate into macrophages if they remained in the sub-endothelial matrix. [6] This work was followed with a validation of these findings in vivo, published one year later in Immunity. [7]

Career and research

In 1998, Randolph became an instructor in the Department of Pathology at Weill Cornell as well as an Adjunct Faculty at The Rockefeller University's Department of Cellular Physiology and Immunology. [1] In 2000, she joined Mount Sinai School of Medicine where she spent 11 years on the faculty in the Department of Gene and Cell Medicine. [8] At Mt. Sinai, her lab explored monocyte fate and differentiation, and their trafficking out of inflamed tissues through lymphatic vessels. [8] One objective was to determine if macrophages could migrate out of organs, via lymphatics or blood, in healthy or diseased states; the laboratory concluded that they do not. [9] [10] Her lab was among the early labs to identify blood monocytes in mice developing a universal method for doing so using expression of CD115, supplanting the far less selective CD11b used to identify myeloid cells more generally. [11] Her lab conducted comparisons of mouse and human monocyte subsets, and created a universal classification nomenclature of myeloid cells. [12]

Randolph moved her lab to Washington University in St. Louis in 2011, studying the role of cholesterol trafficking in diseases such as atherosclerosis and more recently, Crohn's Disease. [13] From 2015 to 2017, she was the Chief of the Division of Immunobiology at Washington University. She is currently the Emil R. Unanue Distinguished Professor in the Department of Pathology and Immunology at Washington University. In 2017, she became the Immunology Graduate Program Director at the School of Medicine and co-director in 2020. [1]

Immunological Genome Project and macrophage diversity

Randolph's lab has contributed to the Immunological Genome Project, a project whose goal is to explore how gene expression relates to immune system function in mice. [14] She spearheaded early work on mouse macrophage gene expression, and her paper published as a part of the Immgen Project is the most highly cited paper of the project. [15]

Lymphatic vasculature and cholesterol trafficking

Randolph's focus changed towards the implications of immune trafficking and lymphatic vasculature in disease processes after moving to Washington University. [16] They showed that lymphatic vessels are critical to the mobilization of cholesterol for excretion and that enhancing lymphatic function might be therapeutic in atherosclerosis. [17] Her lab then showed that collecting lymphatic vessels (CLVs) are involved in the immune response by acting as a site for macrophages and dendritic cells to uptake antigens. The results emphasized that CLVs are important in the coordination of immune responses surrounding adipose depots. [18]  In 2018, her team found that skin-driven immune responses can cause systemic changes that affect the ability of cholesterol to be taken in by tissues thus promoting plaque build-up in arteries around the heart. [19] Specifically, they found that Th17 cells drive the collagen mediated changes seen in experimental psoriasis, and that blocking IL17 rescues cholesterol transport and reduces vascular stiffness. [19]

In 2015, Randolph was awarded the National Institutes of Health Director's 2015 Pioneer Award to pursue high risk-high reward research to study the role of lymphatics and cellular transport in inflammatory bowel disease [16] in collaboration with gastroenterologist, Jean-Frederic Colombel, . [16] [1] In order to understand if damage to lymphatic collecting vessels might contribute to human disease, as it has been shown to do in mice, Randolph's lab developed a three-dimensional imaging approach to explore lymphatic vasculature abnormalities in human mesenteric tissue. [20] This novel approach has allowed them to identify novel tertiary lymphoid organs along the collecting lymphatic vessels that are likely involved in aberrant delivery of lymph to lymph nodes. [20]

Personal life

Randolph is now married to Hermann Kyrychenko and has two children. [1]

Select publications

Related Research Articles

<span class="mw-page-title-main">Lymphatic system</span> Organ system in vertebrates

The lymphatic system, or lymphoid system, is an organ system in vertebrates that is part of the immune system, and complementary to the circulatory system. It consists of a large network of lymphatic vessels, lymph nodes, lymphoid organs, lymphoid tissues and lymph. Lymph is a clear fluid carried by the lymphatic vessels back to the heart for re-circulation..

<span class="mw-page-title-main">Lymph node</span> Organ of the lymphatic system

A lymph node, or lymph gland, is a kidney-shaped organ of the lymphatic system and the adaptive immune system. A large number of lymph nodes are linked throughout the body by the lymphatic vessels. They are major sites of lymphocytes that include B and T cells. Lymph nodes are important for the proper functioning of the immune system, acting as filters for foreign particles including cancer cells, but have no detoxification function.

<span class="mw-page-title-main">Dendritic cell</span> Accessory cell of the mammalian immune system

A dendritic cell (DC) is an antigen-presenting cell of the mammalian immune system. A DC's main function is to process antigen material and present it on the cell surface to the T cells of the immune system. They act as messengers between the innate and adaptive immune systems.

<span class="mw-page-title-main">Macrophage</span> Type of white blood cell

Macrophages are a type of white blood cell of the innate immune system that engulf and digest pathogens, such as cancer cells, microbes, cellular debris, and foreign substances, which do not have proteins that are specific to healthy body cells on their surface. This process is called phagocytosis, which acts to defend the host against infection and injury.

<span class="mw-page-title-main">Phagocyte</span> Cells that ingest harmful matter within the body

Phagocytes are cells that protect the body by ingesting harmful foreign particles, bacteria, and dead or dying cells. Their name comes from the Greek phagein, "to eat" or "devour", and "-cyte", the suffix in biology denoting "cell", from the Greek kutos, "hollow vessel". They are essential for fighting infections and for subsequent immunity. Phagocytes are important throughout the animal kingdom and are highly developed within vertebrates. One litre of human blood contains about six billion phagocytes. They were discovered in 1882 by Ilya Ilyich Mechnikov while he was studying starfish larvae. Mechnikov was awarded the 1908 Nobel Prize in Physiology or Medicine for his discovery. Phagocytes occur in many species; some amoebae behave like macrophage phagocytes, which suggests that phagocytes appeared early in the evolution of life.

<span class="mw-page-title-main">Monocyte</span> Subtype of leukocytes

Monocytes are a type of leukocyte or white blood cell. They are the largest type of leukocyte in blood and can differentiate into macrophages and monocyte-derived dendritic cells. As a part of the vertebrate innate immune system monocytes also influence adaptive immune responses and exert tissue repair functions. There are at least three subclasses of monocytes in human blood based on their phenotypic receptors.

In immunology, the mononuclear phagocyte system or mononuclear phagocytic system (MPS) also known as the reticuloendothelial system or macrophage system is a part of the immune system that consists of the phagocytic cells located in reticular connective tissue. The cells are primarily monocytes and macrophages, and they accumulate in lymph nodes and the spleen. The Kupffer cells of the liver and tissue histiocytes are also part of the MPS. The mononuclear phagocyte system and the monocyte macrophage system refer to two different entities, often mistakenly understood as one.

A histiocyte is a vertebrate cell that is part of the mononuclear phagocyte system. The mononuclear phagocytic system is part of the organism's immune system. The histiocyte is a tissue macrophage or a dendritic cell. Part of their job is to clear out neutrophils once they've reached the end of their lifespan.

<span class="mw-page-title-main">Antigen-presenting cell</span> Cell that displays antigen bound by MHC proteins on its surface

An antigen-presenting cell (APC) or accessory cell is a cell that displays antigen bound by major histocompatibility complex (MHC) proteins on its surface; this process is known as antigen presentation. T cells may recognize these complexes using their T cell receptors (TCRs). APCs process antigens and present them to T-cells.

Gut-associated lymphoid tissue (GALT) is a component of the mucosa-associated lymphoid tissue (MALT) which works in the immune system to protect the body from invasion in the gut.

Malignant histiocytosis is a rare hereditary disease found in the Bernese Mountain Dog and humans, characterized by histiocytic infiltration of the lungs and lymph nodes. The liver, spleen, and central nervous system can also be affected. Histiocytes are a component of the immune system that proliferate abnormally in this disease. In addition to its importance in veterinary medicine, the condition is also important in human pathology.

<span class="mw-page-title-main">Follicular dendritic cells</span> Immune cells found in lymph nodes

Follicular dendritic cells (FDC) are cells of the immune system found in primary and secondary lymph follicles of the B cell areas of the lymphoid tissue. Unlike dendritic cells (DC), FDCs are not derived from the bone-marrow hematopoietic stem cell, but are of mesenchymal origin. Possible functions of FDC include: organizing lymphoid tissue's cells and microarchitecture, capturing antigen to support B cell, promoting debris removal from germinal centers, and protecting against autoimmunity. Disease processes that FDC may contribute include primary FDC-tumor, chronic inflammatory conditions, HIV-1 infection development, and neuroinvasive scrapie.

<span class="mw-page-title-main">Monoblast</span>

Monoblasts are the committed progenitor cells that differentiated from a committed macrophage or dendritic cell precursor (MDP) in the process of hematopoiesis. They are the first developmental stage in the monocyte series leading to a macrophage. Their myeloid cell fate is induced by the concentration of cytokines they are surrounded by during development. These cytokines induce the activation of transcription factors which push completion of the monoblast's myeloid cell fate. Monoblasts are normally found in bone marrow and do not appear in the normal peripheral blood. They mature into monocytes which, in turn, develop into macrophages. They then are seen as macrophages in the normal peripheral blood and many different tissues of the body. Macrophages can produce a variety of effector molecules that initiate local, systemic inflammatory responses. These monoblast differentiated cells are equipped to fight off foreign invaders using pattern recognition receptors to detect antigen as part of the innate immune response.

Certain sites of the mammalian body have immune privilege, meaning they are able to tolerate the introduction of antigens without eliciting an inflammatory immune response. Tissue grafts are normally recognised as foreign antigens by the body and attacked by the immune system. However, in immune privileged sites, tissue grafts can survive for extended periods of time without rejection occurring. Immunologically privileged sites include:

In immunology, peripheral tolerance is the second branch of immunological tolerance, after central tolerance. It takes place in the immune periphery. Its main purpose is to ensure that self-reactive T and B cells which escaped central tolerance do not cause autoimmune disease. Peripheral tolerance prevents immune response to harmless food antigens and allergens, too.

<span class="mw-page-title-main">C-C chemokine receptor type 7</span> Protein-coding gene in the species Homo sapiens

C-C chemokine receptor type 7 is a protein that in humans is encoded by the CCR7 gene. Two ligands have been identified for this receptor: the chemokines ligand 19 (CCL19/ELC) and ligand 21 (CCL21). The ligands have similar affinity for the receptor, though CCL19 has been shown to induce internalisation of CCR7 and desensitisation of the cell to CCL19/CCL21 signals. CCR7 is a transmembrane protein with 7 transmembrane domains, which is coupled with heterotrimeric G proteins, which transduce the signal downstream through various signalling cascades. The main function of the receptor is to guide immune cells to immune organs by detecting specific chemokines, which these tissues secrete.

<span class="mw-page-title-main">GPR183</span> Protein-coding gene in the species Homo sapiens

G-protein coupled receptor 183 also known as Epstein-Barr virus-induced G-protein coupled receptor 2 (EBI2) is a protein (GPCR) expressed on the surface of some immune cells, namely B cells and T cells; in humans it is encoded by the GPR183 gene. Expression of EBI2 is one critical mediator of immune cell localization within lymph nodes, responsible in part for the coordination of B cell, T cell, and dendritic cell movement and interaction following antigen exposure. EBI2 is a receptor for oxysterols. The most potent activator is 7α,25-dihydroxycholesterol (7α,25-OHC), with other oxysterols exhibiting varying affinities for the receptor. Oxysterol gradients drive chemotaxis, attracting the EBI2-expressing cells to locations of high ligand concentration. The GPR183 gene was identified due to its upregulation during Epstein-Barr virus infection of the Burkitt's lymphoma cell line BL41, hence its name: EBI2.

Lymph node stromal cells are essential to the structure and function of the lymph node whose functions include: creating an internal tissue scaffold for the support of hematopoietic cells; the release of small molecule chemical messengers that facilitate interactions between hematopoietic cells; the facilitation of the migration of hematopoietic cells; the presentation of antigens to immune cells at the initiation of the adaptive immune system; and the homeostasis of lymphocyte numbers. Stromal cells originate from multipotent mesenchymal stem cells.

Miram Merad is a French-Algerian professor in Cancer immunology and the Director of the Marc and Jennifer Lipschultz Precision Immunology Institute (PrIISM) at the Icahn School of Medicine at Mount Sinai (ISMMS) in New York, NY. She is the corecipient of the 2018 William B. Coley Award for Distinguished Research in Basic Immunology and a member of the United States National Academy of Sciences and the National Academy of Medicine.

Melanie Greter is a Swiss neuroimmunologist and a Swiss National Science Foundation Professor in the Institute of Experimental Immunology at the University of Zurich. Greter explores the ontogeny and function of microglia and border-associated macrophages of the central nervous system to understand how they maintain homeostasis and contribute to brain-related diseases.

References

  1. 1 2 3 4 5 6 7 8 9 10 "Washington People: Gwen Randolph". Washington University School of Medicine in St. Louis. 2019-09-17. Retrieved 2020-12-31.
  2. 1 2 3 Williams, Neoma; Correspondent, Herald (2017-09-22). "Hart grad Dr. Gwen Wilson is distinguished medical school professor". Plainview Herald. Retrieved 2020-12-31.
  3. "2020 Inflammation Co-Chair". www.navbo.org. Retrieved 2020-12-31.[ permanent dead link ]
  4. "Mononuclear Phagocytes Egress from an In Vitro Mode of the Vascular Wall by Migrating across Endothelium in the Basal to Apical Direction: Role of Intercellular Adhesion Molecule 1 and the CD11/CD18 Integrins" (PDF). core.ac.uk/. February 1996. Retrieved December 31, 2020.
  5. Randolph, Gwendalyn J.; Angeli, Veronique; Swartz, Melody A. (August 2005). "Dendritic-cell trafficking to lymph nodes through lymphatic vessels". Nature Reviews Immunology. 5 (8): 617–628. doi:10.1038/nri1670. ISSN   1474-1741. PMID   16056255. S2CID   28795897.
  6. 1 2 3 Randolph, Gwendalyn J.; Beaulieu, Sylvie; Lebecque, Serge; Steinman, Ralph M.; Muller, William A. (1998-10-16). "Differentiation of Monocytes into Dendritic Cells in a Model of Transendothelial Trafficking". Science. 282 (5388): 480–483. Bibcode:1998Sci...282..480R. doi:10.1126/science.282.5388.480. ISSN   0036-8075. PMID   9774276.
  7. Randolph, Gwendalyn J.; Inaba, Kayo; Robbiani, Davide F.; Steinman, Ralph M.; Muller, William A. (1999-12-01). "Differentiation of Phagocytic Monocytes into Lymph Node Dendritic Cells In Vivo". Immunity. 11 (6): 753–761. doi: 10.1016/S1074-7613(00)80149-1 . ISSN   1074-7613. PMID   10626897.
  8. 1 2 "NIH VideoCast - Macrophages and lymphatics: guardians of the tissue microenvironment". videocast.nih.gov. 21 February 2018. Retrieved 2020-12-31.
  9. Potteaux, Stephane; Gautier, Emmanuel L.; Hutchison, Susan B.; van Rooijen, Nico; Rader, Daniel J.; Thomas, Michael J.; Sorci-Thomas, Mary G.; Randolph, Gwendalyn J. (May 2011). "Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/- mice during disease regression". The Journal of Clinical Investigation. 121 (5): 2025–2036. doi:10.1172/JCI43802. ISSN   1558-8238. PMC   3083793 . PMID   21505265.
  10. Gautier, Emmanuel L.; Ivanov, Stoyan; Lesnik, Philippe; Randolph, Gwendalyn J. (2013-10-10). "Local apoptosis mediates clearance of macrophages from resolving inflammation in mice". Blood. 122 (15): 2714–2722. doi:10.1182/blood-2013-01-478206. ISSN   1528-0020. PMC   3795463 . PMID   23974197.
  11. Qu, Chunfeng; Edwards, Emmerson W.; Tacke, Frank; Angeli, Véronique; Llodrá, Jaime; Sanchez-Schmitz, Guzman; Garin, Alexandre; Haque, Nasreen S.; Peters, Wendy; van Rooijen, Nico; Sanchez-Torres, Carmen (2004-11-15). "Role of CCR8 and Other Chemokine Pathways in the Migration of Monocyte-derived Dendritic Cells to Lymph Nodes". The Journal of Experimental Medicine. 200 (10): 1231–1241. doi:10.1084/jem.20032152. ISSN   0022-1007. PMC   2211916 . PMID   15534368.
  12. Ziegler-Heitbrock, Loems; Ancuta, Petronela; Crowe, Suzanne; Dalod, Marc; Grau, Veronika; Hart, Derek N.; Leenen, Pieter J. M.; Liu, Yong-Jun; MacPherson, Gordon; Randolph, Gwendalyn J.; Scherberich, Juergen (2010-10-21). "Nomenclature of monocytes and dendritic cells in blood". Blood. 116 (16): e74–e80. doi:10.1182/blood-2010-02-258558. hdl: 11379/41075 . ISSN   0006-4971. PMID   20628149. S2CID   1570404.
  13. "Randolph to receive NIH director's Pioneer Award | The Source | Washington University in St. Louis". The Source. 2015-10-06. Retrieved 2020-12-31.
  14. Aguilar, Stephanie Vargas; Aguilar, Oscar; Allan, Rhys; Amir, El Ad David; Angeli, Veronique; Artyomov, Maxim N.; Asinovski, Natasha; Astarita, Jilian; Austen, K. Frank; Bajpai, Geetika; Barrett, Nora (July 2020). "ImmGen at 15". Nature Immunology. 21 (7): 700–703. doi: 10.1038/s41590-020-0687-4 . ISSN   1529-2916. PMID   32577013. S2CID   219988250.
  15. 1 2 Gautier, Emmanuel L.; Shay, Tal; Miller, Jennifer; Greter, Melanie; Jakubzick, Claudia; Ivanov, Stoyan; Helft, Julie; Chow, Andrew; Elpek, Kutlu G.; Gordonov, Simon; Mazloom, Amin R. (November 2012). "Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages". Nature Immunology. 13 (11): 1118–1128. doi:10.1038/ni.2419. ISSN   1529-2916. PMC   3558276 . PMID   23023392.
  16. 1 2 3 Health (2015-11-13). "The Journey from Innovator to Pioneer". Kenneth Rainin Foundation. Retrieved 2020-12-31.
  17. Martel, Catherine; Li, Wenjun; Fulp, Brian; Platt, Andrew M.; Gautier, Emmanuel L.; Westerterp, Marit; Bittman, Robert; Tall, Alan R.; Chen, Shu-Hsia; Thomas, Michael J.; Kreisel, Daniel (April 2013). "Lymphatic vasculature mediates macrophage reverse cholesterol transport in mice". The Journal of Clinical Investigation. 123 (4): 1571–1579. doi:10.1172/JCI63685. ISSN   1558-8238. PMC   3613904 . PMID   23524964.
  18. 1 2 Kuan, Emma L.; Ivanov, Stoyan; Bridenbaugh, Eric A.; Victora, Gabriel; Wang, Wei; Childs, Ed W.; Platt, Andrew M.; Jakubzick, Claudia V.; Mason, Robert J.; Gashev, Anatoliy A.; Nussenzweig, Michel (2015-06-01). "Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node-homing adipose tissue dendritic cells". Journal of Immunology. 194 (11): 5200–5210. doi:10.4049/jimmunol.1500221. ISSN   1550-6606. PMC   4433841 . PMID   25917096.
  19. 1 2 "Link between autoimmune, heart disease explained in mice". Washington University School of Medicine in St. Louis. 2018-11-08. Retrieved 2020-12-31.
  20. 1 2 Randolph, Gwendalyn J.; Bala, Shashi; Rahier, Jean-François; Johnson, Michael W.; Wang, Peter L.; Nalbantoglu, ILKe; Dubuquoy, Laurent; Chau, Amélie; Pariente, Benjamin; Kartheuser, Alex; Zinselmeyer, Bernd H. (December 2016). "Lymphoid Aggregates Remodel Lymphatic Collecting Vessels that Serve Mesenteric Lymph Nodes in Crohn Disease". The American Journal of Pathology. 186 (12): 3066–3073. doi:10.1016/j.ajpath.2016.07.026. ISSN   1525-2191. PMC   5225286 . PMID   27746181.
  21. Huang, Li-Hao; Zinselmeyer, Bernd H.; Chang, Chih-Hao; Saunders, Brian T.; Elvington, Andrew; Baba, Osamu; Broekelmann, Thomas J.; Qi, Lina; Rueve, Joseph S.; Swartz, Melody A.; Kim, Brian S. (5 February 2019). "Interleukin-17 Drives Interstitial Entrapment of Tissue Lipoproteins in Experimental Psoriasis". Cell Metabolism. 29 (2): 475–487.e7. doi:10.1016/j.cmet.2018.10.006. ISSN   1932-7420. PMC   6365189 . PMID   30415924.
  22. Jakubzick, Claudia; Gautier, Emmanuel L.; Gibbings, Sophie L.; Sojka, Dorothy K.; Schlitzer, Andreas; Johnson, Theodore E.; Ivanov, Stoyan; Duan, Qiaonan; Bala, Shashi; Condon, Tracy; van Rooijen, Nico (2013-09-19). "Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes". Immunity. 39 (3): 599–610. doi:10.1016/j.immuni.2013.08.007. ISSN   1097-4180. PMC   3820017 . PMID   24012416.
  23. Randolph, Gwendalyn J.; Sanchez-Schmitz, Guzman; Liebman, Ronald M.; Schäkel, Knut (2002-08-19). "The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting". The Journal of Experimental Medicine. 196 (4): 517–527. doi:10.1084/jem.20011608. ISSN   0022-1007. PMC   2196052 . PMID   12186843.
  24. Randolph, G. J.; Furie, M. B. (1996-02-01). "Mononuclear phagocytes egress from an in vitro model of the vascular wall by migrating across endothelium in the basal to apical direction: role of intercellular adhesion molecule 1 and the CD11/CD18 integrins". The Journal of Experimental Medicine. 183 (2): 451–462. doi:10.1084/jem.183.2.451. ISSN   0022-1007. PMC   2192453 . PMID   8627158.