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Enhanced detection, maintenance, and differentiation of primitive human
hematopoietic cells in cultures containing murine fibroblasts engineered to
produce human steel factor, interleukin-3, and granulocyte
colony-stimulating factor
DE Hogge, PM Lansdorp, D Reid, B Gerhard and CJ Eaves
Terry Fox Laboratory, British Columbia Cancer Agency, Vancouver, Canada.
To determine whether the sensitivity of the human long-term culture-
initiating cell (LTC-IC) assay could be increased, we have evaluated a
spectrum of different fibroblast cell lines for their abilities to
influence the number of cells detectable as LTC-IC, to influence LTC-IC
maintenance, and/or to influence LTC-IC differentiation into colony-
forming cells (CFC) in cocultures containing various sources of LTC-IC. In
a series of initial experiments with highly purified subpopulations of
CD34+ cells from normal human marrow, no significant difference could be
found between any of 3 different murine stromal fibroblast cells in terms
of their support of either LTC-IC detection (CFC production) or maintenance
(over a 6-week period), and all were equivalent to primary human marrow
feeders (HMF). On the other hand, murine M2-10B4 fibroblasts engineered to
produce high levels of both human granulocyte colony-stimulating factor
(G-CSF) and interleukin-3 (IL-3; 190 and 4 ng/mL, respectively), either
alone or mixed 1:1 with SI/SI fibroblasts engineered to produce high levels
of soluble Steel factor (SF), with or without production of the
transmembrane form of SF (60 and 4 ng/ mL, respectively), stimulated the
production of up to 20- fold more CFC in LTC of cells from normal human
marrow, G-CSF-mobilized blood or cord blood when compared with parallel
cocultures containing HMF. Limiting dilution analysis of the CFC output
from all three sources of LTC-IC showed that most of this increase was due
to an ability of the engineered feeders to increase the plating efficiency
of the LTC-IC assay (approximately 14-fold for marrow LTC-IC and
approximately 4-fold for cord blood or mobilized blood LTC-IC). Analysis of
the phenotype of these additionally recruited LTC-IC from marrow showed
they had the same primitive CD34+CD45RA-CD71- phenotype as conventionally
defined LTC-IC. The limiting dilution studies also showed that the average
number of CFC produced per LTC-IC was additionally and independently
increased to yield values of 18 CFC per LTC-IC in marrow, 28 for LTC-IC in
cord blood, and 25 for LTC-IC in G- CSF-mobilized blood. Replating of cells
from primary LTC with different feeders into secondary LTC-IC assays
containing the best combination of engineered feeders showed that LTC-IC
maintenance could be significantly enhanced (up to 7-fold as compared with
primary cocultures containing HMF). However, this enhancement was still not
sufficient to amplify the number of LTC-IC present after 6 weeks above the
input value. Thus, engineering murine fibroblasts to produce sufficient SF,
G-CSF, and IL-3 can markedly enhance the detection as well as the
maintenance in vitro of a very primitive population of human progenitor
cells present in normal adult marrow, mobilized blood, and cord blood by
providing the most sensitive assay conditions thus far described. The
present findings also provide new evidence of biologic heterogeneity
between different cell populations that can be operationally identified as
LTC-IC, thus re-emphasizing the importance of limiting dilution analyses to
distinguish between quantitative and qualitative effects on these cells.
Volume 88,
Issue 10,
pp. 3765-3773,
11/15/1996
Copyright © 1996 by The American Society of Hematology
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4698 - 4703.
[Abstract]
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