METAZOAN CELLS LACK THE CELL
AUTONOMOUS ABILITY TO TAKE
UP NUTRIENTS
Over the last decade, we have been studying the de-
pendency of cells on lineage-specific growth factors. Al-
though this paper focuses on hematopoietic cells, addi-
tional data suggest that the findings are equally true of
neuronal cells, epithelial cells, and fibroblasts. In all of
these cells, the lineage-specific receptors that promote
cell survival regulate the ability of the cell to express the
transporters needed to take up nutrients from the extra-
cellular environment. Every cell in the human body has
an adequate supply of extracellular nutrients to maintain
its survival. However, it appears that the cells in multi-
cellular organisms lack the cell-autonomous ability to
take up nutrients from the extracellular space. For exam-
ple, glucose uptake depends on signal transduction that
directs the cell to produce glucose transporters, hexoki-
nase, and phosphofructokinase (Vander Heiden et al.
2001). These proteins are required to maintain the supply
of glucose utilized by the glycolytic pathway to produce
substrates for mitochondrial oxidative phosphorylation.
When a cell is deprived of survival signals, the ability of
the cell to take up, capture, and metabolize sufficient nu-
trients to maintain ATP production disappears. In every
cell lineage in which this experiment has been done, after
48–96 hours in the absence of the signal transduction that
maintains nutrient uptake and metabolism, the cell initi-
ates apoptosis. This apoptotic response depends on the
activity of the proapoptotic Bcl-2-related proteins, Bax
and Bak (see, e.g., Lindsten et al. 2000).
Bcl-2 PROTEINS REGULATE THE DURATION
OF CELL SURVIVAL FOLLOWING GROWTH
FACTOR WITHDRAWAL
The first question we have addressed concerns the role
of antiapoptotic Bcl-2 proteins in maintaining cell sur-
vival following growth factor withdrawal. Surprisingly,
we found that Bcl-2 proteins play no role in regulating
nutrient uptake. Cells overexpressing antiapoptotic Bcl-2
family members such as Bcl-2 and Bcl-x
L
still need sur-
vival signal transduction to maintain nutrient trans-
porters. For example, interleukin-3 (IL-3)-dependent
cells deprived of IL-3 lose the ability to express both glu-
cose and amino acid transporters. Despite this, antiapo-
ptotic Bcl-2 proteins can keep the cell alive several weeks
in the absence of nutrient transporter expression (Rath-
mell et al. 2000).
Alternative explanations for the decline of nutrient
transporters following growth factor withdrawal have
been suggested. For example, it could be that the decline
in transporters results simply from the cell withdrawing
from the cell cycle and no longer requiring a high level of
nutrients to support growth. This concept would suggest
that changes in nutrient transporter expression are a com-
pensatory response to withdrawal from the cell cycle. In
this view, survival receptors regulate cell survival
through altering the expression/function of Bcl-2 family
members. If Bax and Bak are in excess, apoptosis is ini-
tiated by cytochrome c release into the cytosol and acti-
vation of caspase 9. If Bcl-2 or other antiapoptotic family
members dominate, the cell can survive for a long period
of time.
How Do Cancer Cells Acquire the Fuel Needed
to Support Cell Growth?
C.B. THOMPSON, D.E. BAUER, J.J. LUM, G. HATZIVASSILIOU, W.-X. ZONG, D. DITSWORTH,
F. ZHAO, M. BUZZAI, AND T. LINDSTEN
Abramson Family Cancer Research Institute, Department of Cancer Biology and Department of Medicine,
University of Pennsylvania, Philadelphia, Pennsylvania 19104
Cold Spring Harbor Symposia on Quantitative Biology, Volume LXX. © 2005 Cold Spring Harbor Laboratory Press 0-87969-773-3. 357
In this paper we consider whether the dependency of metazoan cells on extracellular signals to maintain cell survival results
in an important barrier that must be overcome during carcinogenesis. It is now generally accepted that a major barrier to can-
cer comes from the inability of cells to enter and progress through the cell cycle in a cell-autonomous fashion. Most of the
oncogenes studied over the last two decades contribute to the ability of the cancer cell to enter and progress through the cell
cycle in the absence of the instructional signals normally imparted by extracellular growth factors. Over the last two decades,
it has begun to be appreciated that there is a second potential barrier to transformation. It appears that all cells in multicellu-
lar organisms need extracellular signals not only to initiate proliferation, but also to maintain cell survival. Every cell in our
body expresses the proteins necessary to execute its own death by apoptosis. A cell will activate this apoptotic program by
default unless it receives signals from the extracellular environment that allow the cell to suppress the apoptotic machinery
it expresses. It now appears that the molecular basis of this suppression lies in the signaling pathways that regulate cellular
nutrient uptake and direct the metabolic fate of those nutrients.