Real-Time Image Analysis of Cells Undergoing Mitotic Catastrophe

Prof. Michael Mackey (mackey@engineering.uiowa.edu)
Biomedical Engineering / Radiology
5013 Seamans Center
335-6058

Dr. Fiorenza Ianzini (fiorenza-ianzini@uiowa.edu)
Department of Radiology
3970 John Pappajohn Pavilion
384-8094


Introduction

Mammalian cells exposed to physical and chemical stresses usually exhibit transient growth delays that lead to an accumulation of cells in S and G2 phases of the cell cycle. Under these conditions, abnormal levels of cyclin B1, a positive regulator of cell division, accumulate in the cell, leading to premature cell division and ultimately resulting in mitotic catastrophe (Mackey, 1993; Swanson et a.l, 1995;Mackey et a.l, 1996; Ianzini and Mackey, 1997; Ianzini et al. 1999). Such untimely entry into mitosis is associated with a previously uncharacterized form of DNA damage that is thought to lead to chromosome instability and may be an initiating event in cell transformation (Ianzini and Mackey, 1998). Although mitotic catastrophe is generally a lethal process, the question still remains whether a small fraction of cells undergoing this process may survive, thus potentially contributing to the destabilization of the genome that is reflected in chromosomal instability. Experiments are underway to determine the fate of cells undergoing mitotic catastrophe following radiation exposure using the Large Scale Digital Cell Analysis System (LSDCAS) at the newly established Real-Time Cell Analysis Facility here at the University of Iowa. LSDCAS is a computer-controlled microscope system that is capable of automatically generating digital movies of over 1000 separate microscope fields over a three-week interval following treatment. LSDCAS is a joint Biomedical Engineering / Radiology venture, where Dr. Ianzini's lab in Radiology contains the microscope systems (and is in fact a full cell culture and biochemistry lab) and analysis is performed using Unix computers in Biomedical Engineering. For this purpose, a high performance, dual processor Compaq AlphaServer running Tru64 Unix located in Biomedical Engineering will be useful in the analysis of images generated by LSDCAS. In addition, four Compaq XP1000 workstations are located in Dr. Mackey's newly renovated lab in Biomedical Engineering and are dedicated to software development for LSDCAS.


Problem Statement

The frequency of radiation-induced chromosome instability has been estimated to be about 1:3300 of the treated cell population after exposure to 8 Gy of X-rays, a treatment which usually kills about 98% of the cells in the population. Note that death in this system is defined in terms of the ability to form a cell colony of more than 50 cells. In order for mitotic catastrophe to contribute to chromosome instability, the surviving fraction of cells undergoing this event must be no less than .015 per surviving cell, thus requiring that 33,000 single cells must be analyzed to reliably detect 10 cells surviving mitotic catastrophe, under the assumption that cells undergoing this process become unstable. This rather large number of cells would require about 33 cells to be analyzed in each of 1,000 microscope fields; it is expected that, on average, about two out of three fields will yield a colony during the three-week interval following irradiation. LSDCAS can acquire the image data for these studies, yet the volume of data produced is overwhelmingly difficult to analyze. This project will provide for automatic segmentation of individual cells in the microscope field images of control and irradiated cell cultures. First, entry of cells into mitosis must be accurately detected. Following cell division, each daughter cell must be identified and analyzed for subsequent cell division. The results of these analyses must then be presented in an easily comprehended form.


Suggested Methods

Software currently exists in LSDCAS for the automatic segmentation of individual cells in microscope fields. The need here is for an algorithm that can determine the success of cell division for a particular cell. It is expected that a multi-threaded approach toward this problem will aid in the achievement of the project goals. Since the criterion used for cell survival is the ability to form a 50-cell colony, the number of threads that must be dispatched for the analysis of a single cell will not be a burden on the multi-processing AlphaServer used in this project. Thus, an algorithm can be developed to track a single cell from one cell division through the next. Then, if two daughter cells are produced, two new threads of execution (using the same algorithm) can be dispatched to follow the daughter cells, with termination of the thread associated with the previous cell generation. Each cell generation can then be described by the results of the analysis performed by its corresponding thread. Cell division can be detected by simultaneously monitoring cell shape (defined as the perimeter / area ratio) and mean cell pixel intensity, as cells round up and become bright at cell division in the phase contrast microscope images. Following cell division, each daughter cell can be identified through a statistical analysis of the segmented dividing cell: successfully dividing cells present an hourglass shape prior to cytokinesis, at which time the two daughter cells separate and establish their own boundaries. Cells undergoing mitotic catastrophe typically round up, vibrate, and then spread out without undergoing cytokinesis. Later, a destabilization of the nucleus occurs, leading to a fragmented texture in the image. Sometimes, cells undergoing mitotic catastrophe temporarily divide, yet later fuse, forming a multinucleated cell. Further, cells undergoing mitotic catastrophe that die present a dramatic cell lysis that can also be distinguished by abrupt changes in mean pixel intensity. All of these features can be used to distinguish between cells undergoing mitotic catastrophe, cells dividing normally, and cells that die. The cell division data so obtained can be organized into a cell pedigree, which is a binary tree used to depict the fate of cell progeny following a particular treatment.


Expected Results

It is expected that this project will provide the means towards obtaining an accurate estimate of the probability of cell death following a variety of toxic treatments. Further, data on the survivability of cells undergoing mitotic catastrophe will rigorously test the hypothesis that a small fraction of cells undergoing this event may survive and contribute to the later appearance of chromosomal instability, a finding that would establish the importance of this mechanism as a potential initiator of cell transformation.


References

  1. Mackey MA: In vitro effects and biological potential of long duration, moderate hyperthermia. In Medical Radiology, Interstitial and Intracavitary Thermoradiotherapy, Springer-Verlag: Berlin, 1993.
  2. Swanson PE, Carroll SB, Zhang XF and Mackey MA: Spontaneous premature chromosome condensation micronucleus formation, and non-apoptotic cell death in heated HeLa S3 cells. Am J Pathol 146, 963-971, 1995.
  3. Mackey MA, Zhang XF, Hunt C, Sullivan S, Blum, J, Laszlo A and Roti Roti JL: Uncoupling of M-phase kinase activation from the completion of S phase by heat shock. Cancer Res 56, 1770-1774, 1996.
  4. Ianzini, F, and Mackey, MA: Spontaneous premature chromosome condensation and mitotic catastrophe following irradiation of HeLa S3 cells. Int J Radiat Biol 72, 409-421, 1997.
  5. Ianzini, F, and Mackey, MA: Delayed DNA damage associated with mitotic catastrophe following X-irradiation of HeLa S3 cells. Mutagenesis 13, 337-344, 1998.
  6. Ianzini, F, Cherubini, R, and Mackey, MA: Mitotic catastrophe induced by exposure of V79 Chinese hamster cells to low energy protons. Int J Radiat Biol 75, 717-723, 1999.