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7 Developmentally Programmed Healing of Chromosomes

Elizabeth H. Blackburn


Chromosome healing is a developmentally programmed process in diverse eukaryotes. In 1887, Boveri reported that in the parasitic nematode Parascaris equorum, the chromosomes in the presomatic cells of early embryos became fragmented and heterochromatin was eliminated. Similar findings were made for other parasitic nematodes: In Ascaris megalocephala (also called Parascaris univalens) the single pair of chromosomes in diploid germ-line cells is broken into more than 40 fragments in the progenitors of the somatic cells at a fixed stage of early embryonic development (for review, see Muller et al. 1991). These fragments must be stabilized, because they are transmitted intact throughout subsequent somatic cell divisions.

Although most organisms do not undergo such extensive chromosome breakage, many exhibit a developmentally regulated response to an accidentally broken chromosome end. In the 1930s, Barbara McClintock showed that in a growing maize plant, when a ring dicentric chromosome was ruptured as its two centromeres separated, the resulting broken ends fused with each other to form a new ring chromosome. Importantly, McClintock made the original observation that this fate of a broken end was not inevitable: Depending on the tissue type and developmental stage, the broken end could lose its tendency to fuse with other broken ends (McClintock 1939), and McClintock concluded that such a broken end had “healed.” The healed end thereby became as permanently stable as any normal telomere through all subsequent nuclear divisions. This implies that a permanent molecular modification of the broken end of the chromosome occurred upon healing. Such healing specifically...

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