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Perspectives CopyTight 0 1997 by the Genetics Society of America Perspectives Anecdotal, Historical And Critical Commentaries on Genetics Edited by James F. Crow and William F. Dove Chromosome Changes in Cell Differentiation Orlando J. Miller Center for Molecular Medicine and Genetics, Wayne State University, Detroit, Michigan 48201 N a recent “Perspectives” article, EEVA THEW the H19 gene. The maternal H19 allele is expressed, I (1995) called attention to a variety of alterations and its cis-acting, nontranslatable RNA product inhibits in chromosomes that occur regularly in differentiating the expression of the maternal alleles of the other three cells, have been known for many years, and are still genes, mash-2, Ins-2, and I@. The paternal H19 allele poorly understood. Theseincludedfacultatiue heterochro- is methylated and notexpressed, so the paternal alleles matinization, polyploidization by endoreduplication, under- of the other three genes are expressed. Imprinting of replication ofsome sequences inpolytene chromosomes, the Inns-2 and I@ genes is disrupted by maternal inheri- and gene amplijication. The related programmed DNA tance of a targeted deletion of the H19 gene and its loss phenomena called chromatin diminutionand chromo- flanking sequence, while paternal inheritance has no some eliminationalso belong tothis group of highly regu- effect, reflecting the normally silent state of the pater- lated developmental chromosomechanges. Here Ishall nal HI 9 allele (LEIGHTONet al. 1995). There is also a briefly review these changes, with particular emphasis cluster of several genes on human chromosome 15 that on thecell and molecular genetic approaches thathave are expressed exclusively on thepaternal chromosome; provided, or could provide, insights into the signaling these may play a role in thePrader-Willi syndrome. One pathways and molecular mechanisms involved. of these genes has only an RNA product (WEVRICKet Facultative heterochromatinization during differenti- al. 1994). It remainsto be seen whether such &acting, ation is widespread in metazoans and is functionally nontranslatable RNAs play a more general role in im- equivalent to programmed DNA loss. The best known printing and facultative heterochromatinization in ver- examples are mammalian X chromosome inactivation tebrates, coccids, or other taxons. (LYON1961) and the inactivation of the paternally de- DNA methylation plays a role in imprinting as well rived set of chromosomes incoccids destined to become as in gene and X chromosome inactivation (CHAILLET males (HUGHES-SCHRADER1948; BROWNand NELSON- et al. 1995). Histone underacetylation may be an even REES 1961). Both involve imprinting,the epigenetic more general mechanism in imprinting and facultative process that leads to differential expression of the two heterochromatinization UEPPESEN1997). While hypera- parental alleles at a locus. When the fragmented chro- cetylation of histones is characteristic of the DNA in mosomes produced by massive doses of ionizing radia- active genes, underacetylation of histones is characteris- tion are transmitted from fatherto son in the mealybug, tic of the inactive micronucleus of Tetrahymena, the each fragment undergoes heterochromatinization,sug- inactive X chromosome of eutherian or metatherian gesting there are multiple cis-acting centers of inactiva- mammals, and the inactive spermatocyte X chromo- tion in these holocentric chromosomes (BROWNand some of the desert locust, Schistocerca gregaria (WOLF NELSON-REES1961). These may contain nuclease-resis- and TURNER1996); surprisingly, this may not be the tant, matrix-associated AT-rich fragments (KHOSW et case for the inactive Xchromosome in the male germ- al. 1996). In contrast,there is a single centerof X- line of the mouse (ARMSTRONG et al. 1997). inactivation in mammals, and inactivation is mediated Programmed DNA loss is a common event in meta- by the cis-acting RNA product of the XISTgene (BROWN zoan differentiation. It mayinvolve whole chromo- et al. 1.991). somes, large or small segments of chromosomes, or Centers of inactivation and cis-acting RNA products precisely defined short sequences. The earliest exam- appear to be involved in at least one other type of im- ples of programmed DNA loss were chromatin diminu- printing. The imprinting of a cluster of four genes on tion in the nematode Ascaris (BOVERI 1887) and chro- mouse chromosome 7 is mediated by one of the four, mosome elimination in the dipteran Sciaridae (METZ 1938). Cell and molecular genetic approacheshave pro- Author mail: [email protected] vided exciting insights into themechanisms responsible Gmc~tir.;146 1-X (May, 1997) 2 0.J. Miller for each of these, as well as those involved in theV(D)J whose ends are then cappedby telomeric GGGGTTTT recombination that assembles diverse functional immu- repeats. Additional rounds of DNA replication produce noglobulin and T-cell receptor genes from segments the mature macronucleus (PRESCO~1994). In Tetrahy- that are separated in the germline genome. This is di- mena thermophila, the degree of polyploidy is only about rected by evolutionarily conserved cisacting heptamer 45C, and only some 15% of the micronuclear genome and nonomer recombination signal sequences flanking is eliminated during macronuclear development. The the segments (TONEGAWA1983). Recognition and deletion process is very precise and involves specific cis- cutting at V(D)J recombination signal sequences re- acting sequences(YAO 1996). InParamecium tetraaurelia, quires the B and T lymphocyte-specific expression of developmental genomicrearrangements also affect two recombination-activating genes, RAG1 and RAG2 mating type determination (MEYERand KELLER 1996). (MCBLANEet al. 1995), but repairof the resultant dou- Chromosome elimination shares a number of fea- ble-strand breaks (DSBs) uses the same enzyme that all tures with chromatin diminution. Both occur at a pre- cells use for repairing DSBs, a DNAdependent protein cise time in early development, bothlead to the elimina- kinase (BLUNTet al. 1995). tion of a large fraction of the germline genome, both Chromatin diminution in Ascaris and Parascaris spe- can be involved in sex determination, and both can cies involvesfragmentation at the third tofifth cleavage occur in thesame organism, as in several primitive agna- divisions of the very large chromosomes then present than hagfish species. In oneof these, Eptatretus okinosea- and elimination of most of the chromatin. The frag- nus, some of the restricted sequences are highly repeti- mentation occurs at specific chromosome breakage re- tive, and there is variation in the number of germline- gions (CBRs) and is followed by the addition of 2-4 kb restricted chromosomes, leading to the suggestion that of telomeric TTAGGT repeats (MULLERet al. 1991). some supernumerary (B) chromosomes are germline- Chromatin diminution takes place at a specific stage in restricted chromosomes that have escaped their pro- the early embryo and occurs in all somatic precursor grammed elimination (KUBOTA et al. 1992, 1993). So- cells. It is prevented in germline cells by cytoplasmic matic elimination of supernumerary chromosomes has factors close to the vegetal pole and can be induced by been described in both plants and animals (DARLING chemical treatment of eggs, suggesting that the inhibi- TON and THOMAS1941; MELANDER1950). In the myr- tory cytoplasmic factors are already present in the zy- micine ant, Leptothoraxspinosior, B chromosomes are gote (ESTEBANet al. 1995). Chromatin diminutionleads usually restricted to the germline of the haploid males, to the eliminationnot only of alldetectable heterochro- although they are rarely seen in the germline of the matin but also of some euchromatic genes. Three sin- diploid females (IMAI1974). Chromosome elimination gle-copy genes were identified inAscaris suum that were is common in several genera of gall midges (Diptera: eliminated from somatic cells by chromatin diminution; Cecidomyidae), such as Miastor, in which there is weak each is clearly related to a gene thatis retained, leading but suggestive evidence linking chromosome elimina- to the suggestion that chromatin diminution is linked tion to partial genome duplication (BREGMAN1975). to partial genome duplication (MULLERet al. 1996). This point could be clarified with chromosome-specific Chromatindiminution has been most extensively libraries (painting probes) for in situ suppression hy- characterized in ciliates and shows considerable varia- bridization (LICHTERet al. 1988; PINKELet al. 1988). tion among the various taxons (PREscOTT 1994; YAO Chromatin diminutionand chromosome elimination 1996; PREER1997). After conjugation and completion have repeatedly led to the evolution of organisms in of the sexual phase of its life cycle,hypotrichous ciliates which the germline contains DNA sequences not pres- such asStylonychia or Euplotes transform a mitotic ent in somatic cells. Since germline-restricted DNA se- copy of the transcriptionally silent micronucleus into a quences are subject only to selective forces operating macronucleus by a process that takes about 4days. The on the germline and gametes, mutations in them will first half of this period is taken up by endoreduplication inactivate any genes not expressed in the germline and and produces polytene chromosomes. An extreme form will drive the evolution of separate germline-specific of precise chromatin diminution then occurs, resulting and soma-specific genomes, whether interspersed on in lossof more than 90%
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