DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Mechanisms Underlying CD4+ Treg Immune Regulation in the Adult: From Experiments to Models

Abstract

To maintain immunological balance the organism has to be tolerant to self while remaining competent to mount an effective immune response against third-party antigens. An important mechanism of this immune regulation involves the action of regulatory T-cell (Tregs). In this mini-review, we discuss some of the known and proposed mechanisms by which Tregs exert their influence in the context of immune regulation, and the contribution of mathematical modeling for these mechanistic studies. These models explore the mechanisms of action of regulatory T cells, and include hypotheses of multiple signals, delivered through simultaneous antigen-presenting cell (APC) conjugation; interaction of feedback loops between APC, Tregs, and effector cells; or production of specific cytokines that act on effector cells. As the field matures, and competing models are winnowed out, it is likely that we will be able to quantify how tolerance-inducing strategies, such as CD4-blockade, affect T-cell dynamics and what mechanisms explain the observed behavior of T-cell based tolerance.

Authors:
 [1];  [1];  [2]
  1. Inst. Gulbenkian de Ciência, Oeira (Portugal); Univ. of Lisbon (Portugal)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
Work for Others (WFO); USDOE
OSTI Identifier:
1396112
Report Number(s):
LA-UR-13-27742
Journal ID: ISSN 1664-3224
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Immunology
Additional Journal Information:
Journal Volume: 4; Journal ID: ISSN 1664-3224
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biological Science

Citation Formats

Caridade, Marta, Graca, Luis, and Ribeiro, Ruy M. Mechanisms Underlying CD4+ Treg Immune Regulation in the Adult: From Experiments to Models. United States: N. p., 2013. Web. doi:10.3389/fimmu.2013.00378.
Caridade, Marta, Graca, Luis, & Ribeiro, Ruy M. Mechanisms Underlying CD4+ Treg Immune Regulation in the Adult: From Experiments to Models. United States. https://doi.org/10.3389/fimmu.2013.00378
Caridade, Marta, Graca, Luis, and Ribeiro, Ruy M. Mon . "Mechanisms Underlying CD4+ Treg Immune Regulation in the Adult: From Experiments to Models". United States. https://doi.org/10.3389/fimmu.2013.00378. https://www.osti.gov/servlets/purl/1396112.
@article{osti_1396112,
title = {Mechanisms Underlying CD4+ Treg Immune Regulation in the Adult: From Experiments to Models},
author = {Caridade, Marta and Graca, Luis and Ribeiro, Ruy M.},
abstractNote = {To maintain immunological balance the organism has to be tolerant to self while remaining competent to mount an effective immune response against third-party antigens. An important mechanism of this immune regulation involves the action of regulatory T-cell (Tregs). In this mini-review, we discuss some of the known and proposed mechanisms by which Tregs exert their influence in the context of immune regulation, and the contribution of mathematical modeling for these mechanistic studies. These models explore the mechanisms of action of regulatory T cells, and include hypotheses of multiple signals, delivered through simultaneous antigen-presenting cell (APC) conjugation; interaction of feedback loops between APC, Tregs, and effector cells; or production of specific cytokines that act on effector cells. As the field matures, and competing models are winnowed out, it is likely that we will be able to quantify how tolerance-inducing strategies, such as CD4-blockade, affect T-cell dynamics and what mechanisms explain the observed behavior of T-cell based tolerance.},
doi = {10.3389/fimmu.2013.00378},
journal = {Frontiers in Immunology},
number = ,
volume = 4,
place = {United States},
year = {Mon Nov 18 00:00:00 EST 2013},
month = {Mon Nov 18 00:00:00 EST 2013}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 45 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Anergy induced by thymic medullary epithelium
journal, July 1992

  • Schönrich, Günther; Momburg, Frank; Hämmerling, Günter J.
  • European Journal of Immunology, Vol. 22, Issue 7
  • DOI: 10.1002/eji.1830220704

Regulation of CD4+CD25+regulatory T cell activity: it takes (IL-)two to tango
journal, April 2005

  • Scheffold, Alexander; Hühn, Jochen; Höfer, Thomas
  • European Journal of Immunology, Vol. 35, Issue 5
  • DOI: 10.1002/eji.200425887

Sub-optimal CD4+ T-cell activation triggers autonomous TGF-β-dependent conversion to Foxp3+ regulatory T cells
journal, April 2011

  • Oliveira, Vanessa G.; Caridade, Marta; Paiva, Ricardo S.
  • European Journal of Immunology, Vol. 41, Issue 5
  • DOI: 10.1002/eji.201040896

Modelling T-cell-Mediated Suppression Dependent on Interactions in Multicellular Conjugates
journal, November 2000

  • LeÓN, Kalet; PerÉZ, Rolando; Lage, Agustin
  • Journal of Theoretical Biology, Vol. 207, Issue 2
  • DOI: 10.1006/jtbi.2000.2169

Self-tolerance and Autoimmunity in a Regulatory T Cell Model
journal, March 2010


The thymus selects the useful, neglects the useless and destroys the harmful
journal, February 1989


The impact of multiple T cell–APC encounters and the role of anergy
journal, December 2005

  • Chan, Cliburn; Stark, Jaroslav; George, Andrew J. T.
  • Journal of Computational and Applied Mathematics, Vol. 184, Issue 1
  • DOI: 10.1016/j.cam.2004.07.036

Immunological self-tolerance: Lessons from mathematical modeling
journal, December 2005

  • Carneiro, Jorge; Paixão, Tiago; Milutinovic, Dejan
  • Journal of Computational and Applied Mathematics, Vol. 184, Issue 1
  • DOI: 10.1016/j.cam.2004.10.025

Human T Regulatory Cells Can Use the Perforin Pathway to Cause Autologous Target Cell Death
journal, October 2004


Granzyme B and Perforin Are Important for Regulatory T Cell-Mediated Suppression of Tumor Clearance
journal, October 2007


Regulatory T Cell-Derived Interleukin-10 Limits Inflammation at Environmental Interfaces
journal, April 2008


Development and Maintenance of Regulatory T cells
journal, March 2013


Dominant tolerance: activation thresholds for peripheral generation of regulatory T cells
journal, March 2005


Inverse correlation between the incidences of autoimmune disease and infection predicted by a model of T cell mediated tolerance
journal, February 2004


A general mathematical framework to model generation structure in a population of asynchronously dividing cells
journal, August 2004


Modeling regulation mechanisms in the immune system
journal, May 2007


How regulatory CD25+CD4+T cells impinge on tumor immunobiology? On the existence of two alternative dynamical classes of tumors
journal, July 2007


Modeling the role of IL-2 in the interplay between CD4+ helper and regulatory T cells: Assessing general dynamical properties
journal, February 2010


Sensibility of the quorum growth thresholds controlling local immune responses
journal, April 2008

  • Burroughs, N. J.; Oliveira, B. M. P. M.; Pinto, A. A.
  • Mathematical and Computer Modelling, Vol. 47, Issue 7-8
  • DOI: 10.1016/j.mcm.2007.06.007

Natural regulatory T cells: mechanisms of suppression
journal, March 2007


Regulatory T cells in transplantation
journal, April 2006


B7/CD28 Costimulation Is Essential for the Homeostasis of the CD4+CD25+ Immunoregulatory T Cells that Control Autoimmune Diabetes
journal, April 2000


Essential requirement for major histocompatibility complex recognition in T-cell tolerance induction
journal, March 1984

  • Lamb, Jonathan R.; Feldmann, Marc
  • Nature, Vol. 308, Issue 5954
  • DOI: 10.1038/308072a0

T-cell receptor Vβ use predicts reactivity and tolerance to Mlsa- encoded antigens
journal, March 1988

  • MacDonald, H. Robson; Schneider, Reto; Lees, Rosemary K.
  • Nature, Vol. 332, Issue 6159
  • DOI: 10.1038/332040a0

Unopposed positive selection and autoreactivity in mice expressing class II MHC only on thymic cortex
journal, September 1996

  • Laufer, Terri M.; DeKoning, Jenefer; Markowitz, Jay S.
  • Nature, Vol. 383, Issue 6595
  • DOI: 10.1038/383081a0

X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy
journal, January 2001

  • Wildin, Robert S.; Ramsdell, Fred; Peake, Jane
  • Nature Genetics, Vol. 27, Issue 1
  • DOI: 10.1038/83707

The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3
journal, January 2001

  • Bennett, Craig L.; Christie, Jacinda; Ramsdell, Fred
  • Nature Genetics, Vol. 27, Issue 1
  • DOI: 10.1038/83713

Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse
journal, January 2001

  • Brunkow, Mary E.; Jeffery, Eric W.; Hjerrild, Kathryn A.
  • Nature Genetics, Vol. 27, Issue 1
  • DOI: 10.1038/83784

Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide
journal, April 2001

  • Jordan, Martha S.; Boesteanu, Alina; Reed, Amy J.
  • Nature Immunology, Vol. 2, Issue 4
  • DOI: 10.1038/86302

CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory T cell differentiation independently of interleukin 2
journal, January 2005

  • Tai, Xuguang; Cowan, Michelle; Feigenbaum, Lionel
  • Nature Immunology, Vol. 6, Issue 2
  • DOI: 10.1038/ni1160

Competition for cytokines: Treg cells take all
journal, December 2007

  • Scheffold, Alexander; Murphy, Kenneth M.; Höfer, Thomas
  • Nature Immunology, Vol. 8, Issue 12
  • DOI: 10.1038/ni1207-1285

A function for interleukin 2 in Foxp3-expressing regulatory T cells
journal, October 2005

  • Fontenot, Jason D.; Rasmussen, Jeffrey P.; Gavin, Marc A.
  • Nature Immunology, Vol. 6, Issue 11
  • DOI: 10.1038/ni1263

Inducing and expanding regulatory T cell populations by foreign antigen
journal, October 2005

  • Kretschmer, Karsten; Apostolou, Irina; Hawiger, Daniel
  • Nature Immunology, Vol. 6, Issue 12
  • DOI: 10.1038/ni1265

Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3− precursor cells in the absence of interleukin 10
journal, August 2007

  • Maynard, Craig L.; Harrington, Laurie E.; Janowski, Karen M.
  • Nature Immunology, Vol. 8, Issue 9
  • DOI: 10.1038/ni1504

Origin of regulatory T cells with known specificity for antigen
journal, July 2002

  • Apostolou, Irina; Sarukhan, Adelaida; Klein, Ludger
  • Nature Immunology, Vol. 3, Issue 8
  • DOI: 10.1038/ni816

Dominant transplantation tolerance impairs CD8+ T cell function but not expansion
journal, November 2002

  • Lin, Chun-Yen; Graca, Luis; Cobbold, Stephen P.
  • Nature Immunology, Vol. 3, Issue 12
  • DOI: 10.1038/ni853

Foxp3 programs the development and function of CD4+CD25+ regulatory T cells
journal, March 2003

  • Fontenot, Jason D.; Gavin, Marc A.; Rudensky, Alexander Y.
  • Nature Immunology, Vol. 4, Issue 4
  • DOI: 10.1038/ni904

An essential role for Scurfin in CD4+CD25+ T regulatory cells
journal, March 2003

  • Khattri, Roli; Cox, Tom; Yasayko, Sue-Ann
  • Nature Immunology, Vol. 4, Issue 4
  • DOI: 10.1038/ni909

The inhibitory function of B7 costimulators in T cell responses to foreign and self-antigens
journal, May 2003

  • Lohr, Jens; Knoechel, Birgit; Jiang, Shuwei
  • Nature Immunology, Vol. 4, Issue 7
  • DOI: 10.1038/ni939

How regulatory T cells work
journal, July 2008

  • Vignali, Dario A. A.; Collison, Lauren W.; Workman, Creg J.
  • Nature Reviews Immunology, Vol. 8, Issue 7
  • DOI: 10.1038/nri2343

Modelling viral and immune system dynamics
journal, January 2002

  • Perelson, Alan S.
  • Nature Reviews Immunology, Vol. 2, Issue 1
  • DOI: 10.1038/nri700

Selection and fine-tuning of the autoimmune T-cell repertoire
journal, July 2002

  • Anderton, Stephen M.; Wraith, David C.
  • Nature Reviews Immunology, Vol. 2, Issue 7
  • DOI: 10.1038/nri842

Donor-specific transplantation tolerance: The paradoxical behavior of CD4+CD25+T cells
journal, June 2004

  • Graca, Luis; Le Moine, Alain; Lin, Chun-Yen
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 27
  • DOI: 10.1073/pnas.0400084101

Infectious tolerance via the consumption of essential amino acids and mTOR signaling
journal, July 2009

  • Cobbold, Stephen P.; Adams, Elizabeth; Farquhar, Claire A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 29
  • DOI: 10.1073/pnas.0903919106

Dendritic cell modulation by 1α,25 dihydroxyvitamin D3and its analogs: A vitamin D receptor-dependent pathway that promotes a persistent state of immaturityin vitroandin vivo
journal, May 2001

  • Griffin, Matthew D.; Lutz, Ward; Phan, Vy A.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 12
  • DOI: 10.1073/pnas.121172198

Adaptive cellular interactions in the immune system: the tunable activation threshold and the significance of subthreshold responses.
journal, November 1992

  • Grossman, Z.; Paul, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 21
  • DOI: 10.1073/pnas.89.21.10365

Explaining high alloreactivity as a quantitative consequence of affinity-driven thymocyte selection
journal, April 1999

  • Detours, Vincent; Perelson, Alan S.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 9
  • DOI: 10.1073/pnas.96.9.5153

Induction of tolerance in influenza virus-immune T lymphocyte clones with synthetic peptides of influenza hemagglutinin.
journal, May 1983

  • Lamb, J. R.; Skidmore, B. J.; Green, N.
  • Journal of Experimental Medicine, Vol. 157, Issue 5
  • DOI: 10.1084/jem.157.5.1434

Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells
journal, July 1996


Interleukin 2 Signaling Is Required for CD4+ Regulatory T Cell Function
journal, September 2002

  • Furtado, Gláucia C.; de Lafaille, Maria A. Curotto; Kutchukhidze, Nino
  • Journal of Experimental Medicine, Vol. 196, Issue 6
  • DOI: 10.1084/jem.20020190

Conversion of Peripheral CD4+CD25− Naive T Cells to CD4+CD25+ Regulatory T Cells by TGF-β Induction of Transcription Factor Foxp3
journal, December 2003

  • Chen, WanJun; Jin, Wenwen; Hardegen, Neil
  • Journal of Experimental Medicine, Vol. 198, Issue 12
  • DOI: 10.1084/jem.20030152

In Vivo Instruction of Suppressor Commitment in Naive T Cells
journal, May 2004

  • Apostolou, Irina; von Boehmer, Harald
  • Journal of Experimental Medicine, Vol. 199, Issue 10
  • DOI: 10.1084/jem.20040249

Conversion of CD4+ CD25− cells into CD4+ CD25+ regulatory T cells in vivo requires B7 costimulation, but not the thymus
journal, January 2005

  • Liang, Shuang; Alard, Pascale; Zhao, Yuan
  • Journal of Experimental Medicine, Vol. 201, Issue 1
  • DOI: 10.1084/jem.20041201

Sequential development of interleukin 2–dependent effector and regulatory T cells in response to endogenous systemic antigen
journal, November 2005

  • Knoechel, Birgit; Lohr, Jens; Kahn, Estelle
  • Journal of Experimental Medicine, Vol. 202, Issue 10
  • DOI: 10.1084/jem.20050855

Sustained suppression by Foxp3+ regulatory T cells is vital for infectious transplantation tolerance
journal, August 2011

  • Kendal, Adrian R.; Chen, Ye; Regateiro, Frederico S.
  • Journal of Experimental Medicine, Vol. 208, Issue 10
  • DOI: 10.1084/jem.20110767

Crucial role of FOXP3 in the development and function of human CD25+CD4+ regulatory T cells
journal, October 2004

  • Yagi, Haruhiko; Nomura, Takashi; Nakamura, Kyoko
  • International Immunology, Vol. 16, Issue 11
  • DOI: 10.1093/intimm/dxh165

Regulatory T cells: how do they suppress immune responses?
journal, September 2009

  • Sakaguchi, S.; Wing, K.; Onishi, Y.
  • International Immunology, Vol. 21, Issue 10
  • DOI: 10.1093/intimm/dxp095

Maximal frustration as an immunological principle
journal, August 2008

  • de Abreu, F. Vistulo; Mostardinha, P.
  • Journal of The Royal Society Interface, Vol. 6, Issue 32
  • DOI: 10.1098/rsif.2008.0280

A stochastic T cell response criterion
journal, June 2012

  • Currie, James; Castro, Mario; Lythe, Grant
  • Journal of The Royal Society Interface, Vol. 9, Issue 76
  • DOI: 10.1098/rsif.2012.0205

Quantitative theories of T-cell responsiveness
journal, March 2007


When three is not a crowd: a Crossregulation Model of the dynamics and repertoire selection of regulatory CD4+T cells
journal, March 2007


Control of Regulatory T Cell Development by the Transcription Factor Foxp3
journal, February 2003


Regulating the Regulators
journal, February 2003


Reciprocal TH17 and Regulatory T Cell Differentiation Mediated by Retinoic Acid
journal, July 2007


A Nondeletional Mechanism of Thymic Self Tolerance
journal, November 1989


"Infectious" Transplantation Tolerance
journal, February 1993


Anergic T Cells as Suppressor Cells in Vitro
journal, June 1994


Regulatory T Cells: Mechanisms of Differentiation and Function
journal, April 2012


Oral tolerance in the absence of naturally occurring Tregs
journal, July 2005

  • Mucida, D.
  • Journal of Clinical Investigation, Vol. 115, Issue 7
  • DOI: 10.1172/jci24487

An obligate cell-intrinsic function for CD28 in Tregs
journal, January 2013

  • Zhang, Ruan; Huynh, Alexandria; Whitcher, Gregory
  • Journal of Clinical Investigation
  • DOI: 10.1172/jci65013

Modeling the effector - regulatory T cell cross-regulation reveals the intrinsic character of relapses in Multiple Sclerosis
journal, July 2011

  • Vélez de Mendizábal, Nieves; Carneiro, Jorge; Solé, Ricard V.
  • BMC Systems Biology, Vol. 5, Issue 1
  • DOI: 10.1186/1752-0509-5-114

Dynamic cross-regulation of antigen-specific effector and regulatory T cell subpopulations and microglia in brain autoimmunity
journal, April 2013

  • Martinez-Pasamar, Sara; Abad, Elena; Moreno, Beatriz
  • BMC Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1752-0509-7-34

Development and function of naturally occurring CD4+CD25+ regulatory T cells
journal, June 2006

  • Toda, Akiko; Piccirillo, Ciriaco A.
  • Journal of Leukocyte Biology, Vol. 80, Issue 3
  • DOI: 10.1189/jlb.0206095

The main function of IL-2 is to promote the development of T regulatory cells
journal, September 2003


In Vivo Dynamical Interactions between CD4 Tregs, CD8 Tregs and CD4+CD25− Cells in Mice
journal, December 2009


Modeling Adaptive Regulatory T-Cell Dynamics during Early HIV Infection
journal, April 2012


CTLs' repertoire shaping in the thymus: A Monte Carlo simulation
journal, January 2011


The Resurrection of T Cell-Mediated Suppression
journal, April 2011


Induction of tolerance by IL-10-treated dendritic cells.
journal, November 1997


Deriving Quantitative Constraints on T Cell Selection from Data on the Mature T Cell Repertoire
journal, January 2000


Cutting Edge: Anti-CD154 Therapeutic Antibodies Induce Infectious Transplantation Tolerance
journal, November 2000


Three-Cell Interactions in T Cell-Mediated Suppression? A Mathematical Analysis of Its Quantitative Implications
journal, May 2001


The Impact of Thymic Antigen Diversity on the Size of the Selected T Cell Repertoire
journal, June 2004


Natural and Induced CD4+CD25+ Cells Educate CD4+CD25− Cells to Develop Suppressive Activity: The Role of IL-2, TGF-β, and IL-10
journal, May 2004


Rapamycin Promotes Expansion of Functional CD4+CD25+FOXP3+ Regulatory T Cells of Both Healthy Subjects and Type 1 Diabetic Patients
journal, December 2006

  • Battaglia, Manuela; Stabilini, Angela; Migliavacca, Barbara
  • The Journal of Immunology, Vol. 177, Issue 12
  • DOI: 10.4049/jimmunol.177.12.8338

A Kinetic and Dynamic Analysis of Foxp3 Induced in T Cells by TGF-β
journal, June 2007


Comment on “Cutting Edge: Induction of B7-H4 on APCs through IL-10: Novel Suppressive Mode for Regulatory T Cells”
journal, April 2007


Works referencing / citing this record:

The Roles of CD4+ T-Cells in Tumor Immunity
book, January 2020

  • Tavakolpour, Soheil; Darvishi, Mohammad; Rezaei, Nima
  • Cancer Immunology: A Translational Medicine Context, p. 63-90
  • DOI: 10.1007/978-3-030-30845-2_5

Correction: Advances in islet encapsulation technologies
journal, May 2017

  • Desai, Tejal; Shea, Lonnie D.
  • Nature Reviews Drug Discovery, Vol. 16, Issue 5
  • DOI: 10.1038/nrd.2017.67

Human regulatory T cells (Treg) and their response to cancer
journal, June 2019


High tumour plasma cell infiltration reflects an important microenvironmental component in classic Hodgkin lymphoma linked to presence of B‐symptoms
journal, January 2018

  • Gholiha, Alex R.; Hollander, Peter; Hedstrom, Gustaf
  • British Journal of Haematology, Vol. 184, Issue 2
  • DOI: 10.1111/bjh.15703

Transcriptional analysis of Foxp3+ Tregs and functions of two identified molecules during resolution of ALI
journal, March 2019


Acute Malaria Induces PD1+CTLA4+ Effector T Cells with Cell-Extrinsic Suppressor Function
journal, November 2016


Biological Activities of Lactose-Derived Prebiotics and Symbiotic with Probiotics on Gastrointestinal System
journal, April 2018


Route of Antigen Presentation Can Determine the Selection of Foxp3-Dependent or Foxp3-Independent Dominant Immune Tolerance
journal, November 2017

  • Agua-Doce, Ana; Caridade, Marta; Oliveira, Vanessa G.
  • The Journal of Immunology, Vol. 200, Issue 1
  • DOI: 10.4049/jimmunol.1601886

Transcriptional analysis of Foxp3+ Tregs and functions of two identified molecules during resolution of ALI
text, January 2019

  • J. R., Martin,; R. S., Hagan,; H., Dang,
  • American Society for Clinical Investigation
  • DOI: 10.17615/9z1w-7842

Advances in islet encapsulation technologies
journal, December 2016

  • Desai, Tejal; Shea, Lonnie D.
  • Nature Reviews Drug Discovery, Vol. 16, Issue 5
  • DOI: 10.1038/nrd.2016.232

Immune System Modeling and Analysis
journal, December 2014


A Novel Model on DST-Induced Transplantation Tolerance by the Transfer of Self-Specific Donor tTregs to a Haplotype-Matched Organ Recipient
journal, February 2017


NOTCH and Graft-Versus-Host Disease
journal, August 2018


Functional Phenotypic Diversity of Regulatory T Cells Remaining in Inflamed Skin
journal, May 2019


Mesenchymal Stromal Cells for Transplant Tolerance
journal, June 2019

  • Podestà, Manuel Alfredo; Remuzzi, Giuseppe; Casiraghi, Federica
  • Frontiers in Immunology, Vol. 10
  • DOI: 10.3389/fimmu.2019.01287