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Blood, Vol. 94 No. 5 (September 1), 1999:
pp. 1590-1600
Lineage-Specific Expression of Human Immunodeficiency Virus (HIV)
Receptor/Coreceptors in Differentiating Hematopoietic Precursors:
Correlation With Susceptibility to T- and M-Tropic HIV and
Chemokine-Mediated HIV Resistance
C. Chelucci,
I. Casella,
M. Federico,
U. Testa,
G. Macioce,
E. Pelosi,
R. Guerriero,
G. Mariani,
A. Giampaolo,
H.J. Hassan, and
C. Peschle
From the Departments of Hematology-Oncology and Virology, Istituto
Superiore di Sanità, Rome, Italy; and Kimmel Cancer Center,
Thomas Jefferson University, Philadelphia, PA.
Human immunodeficiency virus (HIV) entry is mediated not only by the
CD4 receptor, but also by interaction with closely related molecules
that act as membrane coreceptors. We have analyzed mRNA expression
and/or cell membrane exposition of the coreceptors most widely used by
diverse HIV-1 strains (CXCR4, CCR5, and CCR3) on purified hematopoietic
progenitor cells (HPCs) induced in liquid suspension culture to
unilineage differentiation/maturation through the erythroid (E),
granulocytic (G), megakaryocytic (Mk), and monocytic (Mo) lineages.
Reverse transcriptase-polymerase chain reaction (RT-PCR) and
cytofluorimetric analysis showed the presence of both CXCR4 and CCR5 in
quiescent HPCs, but failed to detect CCR3-specific transcripts.
Chemokine expression in HPC progenies showed that CXCR4 receptor is
detected on the majority of MKs from early to late stages of
maturation, whereas it is moderately decreased in the Mo lineage. In
the G pathway, two distinct cell populations, CXCR4+ and
CXCR4 , were observed: morphological analysis of the
sorted populations showed that the CXCR4+ cells were
largely eosinophils and the CXCR4 were granulocytes of
the neutrophilic series. Furthermore, in the E pathway, CXCR4 was
almost completely absent. CCR5 expression is restricted to Mo cultures,
ie,  30% to 80% cells throughout all monocytopoietic
differentiation/maturation stages. Finally, CCR3 mRNA is always absent
in all the unilineage cultures. Evaluation of CD4 expression by flow
cytometry on both quiescent HPCs and differentiating unilineage
precursors showed that the CD4 receptor is present on 15% of the
starting CD34+ HPC population, highly expressed in the Mo
lineage up to 80% at terminal maturation, present on 20% to 30% of
maturing Mks, and not detectable in either the E or G lineage.
Expression of CD4 receptor together with CXCR4 and/or CCR5 coreceptor
in the four lineages correlates with hematopoietic precursor
susceptibility to T-lymphotropic and macrophage (M)-tropic HIV strains
infection: (1) CD4 G and E cells were resistant to both
M-tropic and T-lymphotropic strains; (2) HPC-derived Mks were
susceptible to T-tropic, but resistant to M-tropic, infection; (3) Mo
differentiating cells efficiently replicate both HIV strains.
Furthermore, we showed that the CXCR4 and CCR5 ligands (stromal-derived
factor 1 and macrophage-inflammatory protein-1 [MIP-1],
MIP-1 and RANTES, respectively) inhibit HIV replication in both
maturing Mo and Mk cells. Taken together, our data show a
lineage-specific modulation of chemokine receptor/coreceptor during
hematopoietic cell differentiation and extend previous observations on
the relationship between the expression of HIV receptor/coreceptors,
susceptibility, and chemokine-mediated resistance to HIV infection.
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