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Prepublished online as a Blood First Edition Paper on June 7, 2002; DOI 10.1182/blood-2001-12-0291.
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Blood, 1 October 2002, Vol. 100, No. 7, pp. 2562-2571
IMMUNOBIOLOGY
Role for granulocyte colony-stimulating factor in the
generation of human T regulatory type 1 cells
Sergio Rutella,
Luca Pierelli,
Giuseppina Bonanno,
Simona Sica,
Franco Ameglio,
Ettore Capoluongo,
Andrea Mariotti,
Giovanni Scambia,
Giuseppe d'Onofrio, and
Giuseppe Leone
From the Departments of Hematology and Gynecology,
Catholic University Medical School, Rome, and the Laboratory of
Clinical Pathology and Microbiology, IRCCS San Gallicano, Rome, Italy.
Granulocyte colony-stimulating factor (G-CSF) may affect
T-cell homeostasis by multiple mechanisms, inducing polarization of
cytokine secretion, inhibition of T-cell proliferation, and enhancement
of T-cell apoptosis. We analyzed the production of interleukin-10
(IL-10) and transforming growth factor- 1 (TGF-1) by T cells from
healthy volunteer donors treated with recombinant human G-CSF. Highly
purified CD4+ T cells obtained before and after G-CSF
administration (pre-G and post-G, respectively) were activated
using the allogeneic mixed leukocyte reaction. Post-G CD4+
T cells produced high levels of IL-10 but undetectable levels of IL-2
and IL-4, whereas the level of TGF-1 release was comparable to that
of pre-G CD4+ T cells. Notably, post-G CD4+ T
cells proliferated poorly in response to alloantigens and to recall
antigens and suppressed the proliferation of autologous CD4+ T cells in a cell contact-independent and an
antigen-nonspecific manner. TGF-1 and IL-10 were not dispensable
for post-G CD4+ T cells to mediate suppression, as shown by
neutralization studies. Compared with pre-G CD4+ T cells,
alloantigen-activated post-G CD4+ T cells preferentially
expressed markers associated with memory T cells, in conjunction with
reduced levels of CD28 and CD62L. Collectively, these data demonstrate
that CD4+ T cells exposed to G-CSF in vivo acquire the
properties of T regulatory (Tr) cells once triggered in vitro through
the T-cell receptor, including a peculiar cytokine production profile
(IL-10++TGF-1+IL-2low/ IL-4low/),
an intrinsic low proliferative capacity, and a contact-independent suppression of antigen-driven proliferation. Tr cells generated ex vivo
after exposure to G-CSF might be clinically relevant for transplantation medicine and for the treatment of human
immune-mediated diseases.
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