ExperimentalGerontology, Vol.27, pp. 383-389, 1992 0531-5565/92 $5.00 + .00
Printed in the USA.All rightsreserved. Copyright© 1992 PergamonPressLtd.
THE TWO-STAGE MECHANISM CONTROLLING CELLULAR
SENESCENCE AND IMMORTALIZATION
WOODRING E. WRIGHT and JERRY W. SHAY
University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, Texas 75235-9039
Key Words: aging, senescence, retinoblastoma gene product, p53, telomeres, life span
INTRODUCTION
IN ORDER for cancer cells to become immortal, they must first escape the controls that
limit the proliferative capacity of all normal diploid cells. We began these experiments
with the hope that understanding the molecular details of immortalization would identify
the key factors involved in establishing the senescent state. The knowledge of these factors
would in turn provide the starting point for studying the programming events that regu-
lated the timing of cellular senescence.
Most of the work on cellular immortalization has come from the identification of a vari-
ety ofoncogenes in rodent cells. Although claims have been made for the identification of
immortalizing nuclear versus "transforming" cytoplasmic oncogenes, virtually all of these
studies have employed some form of clonal or focus-forming assay. The functions that
have been examined can thus be reinterpreted as those that increase the clonability of cells
or their ability to overcome contact inhibition of cell growth, rather than those that directly
cause immortalization. The very high spontaneous rate of immortalization in mouse cells
could then account for an immortalization event occurring in the expanded population of
cells produced as a result of the oncogene, with the eventual production of a truly immortal
population.
Although carcinogens, mutagens, and oncogenes increase the rate of immortalization
in rodent cells, none of these have been found to be effective in human cells. The only
agents that are known rarely but consistently to immortalize human diploid fibroblasts are
DNA tumor viruses such as simian virus 40 (SV40), adenovirus, and the human papilloma
virus. Even these tumor viruses fail to directly immortalize human cells. Rather, they first
confer an increased growth rate and abnormal morphology, aneuploidy rapidly develops,
and the cells eventually enter a state called crisis. During crisis, the rate of cell division and
cell death are initially balanced so that the population size remains constant. Later, divi-
sion decreases and death increases, with the result that the culture is lost. In rare cases, a
Correspondence to: W.E. Wright, Department of Cell Biology and Neuroscience, U.T. Southwestern Medical
Center, 5323 Harry Hines Blvd., Dallas, TX 75235-9039.
383