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Developmental capacities of benign and malignant neoplasms ofDrosophila

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Summary

The developmental properties of three neoplasms found in lethal mutants ofDrosophila melanogaster were studied and compared with the development of the corresponding wild-type organs. Two of these neoplasms are found in the late larval lethal mutant,lethal (2) giant larvae 4 (l(2)gl 4) and its allele,lethal (2) giant larvae (l(2)gl). The third neoplasm occurs in the hemizygous lethal male embryos of the mutantNotch 8 (Df(1)N 8).

The mutantsl(2)gl 4 andl(2)gl were shown to possess defects involving imaginal primordia of ectodermal origin, such as the imaginal discs of the adult integument and the imaginal optic primordia in the larval brain. They also have enlarged lymph glands and abnormal gonads, salivary and ring glands. Thel(2)gl 4 andl(2)gl mutations transform the imaginal discs into noninvasive, lethal neoplasms and the imaginal optic primordia in the larval brain into an invasive and lethal neuroblastoma. Both neoplasms were serially subcultured in female adult hosts where they grew rapidly and killed their hosts in 7–14 days. The neoplastic development of thel(2)gl 4 imaginal discs and brain proved autonomous at all stages that were investigated from 10 hour old embryos to mature larvae. When exposed to the hormonal conditions of metamorphosis, the neoplastic tissues,in situ as well as those that had been culturedin vivo, ceased to grow but failed to metamorphose into parts of the adult integument or brain. Furthermore, in almost all cases they failed to resume their growth in the adult fly after metamorphosis.

Thel(2)gl 4 brain neuroblastoma changed after prolonged subculturein vivo so that although the cells stopped dividing temporarily at the time of metamorphosis of the host, they resumed their growth shortly thereafter and continued to divide throughout adult development and in the emerged adult. Many of thel(2)gl 4 neuroblastoma cells showed abnormal karyotypes, shapes and sizes after prolonged culturein vivo.

Thel(2)gl 4 imaginal disc tissue resembles, in both structure and behavior, certain atelotypic tissue sublines which arise from wild-type imaginal discs after prolonged culturein vivo: the ultrastructure of both types of cells are similar and both cease to grow when exposed to hormonal conditions of metamorphosis. Apparently the epigenetic processes which transform wild-type imaginal discs afterin vivo subculture into atelotypic neoplasms have the same phenotypic expression as the genetic processes at work inl(2)gl 4 imaginal discs.

An analysis of several other late larval and larval-pupal mutants with defective imaginal discs, such asl(2)gd andl(1)d.lg.-1 revealed that they also had defects in parts of the brain destined to form adult structures. This observation indicates that mutations that affect imaginal discs of the adult integument also affect the imaginal primordia of the adult brain.

The neoplasm in the hemizygous male embryo of the embryonic lethalNotch 8 is a teratoma-like growth which is lethal and invasive; when implanted into female adult hosts it gives rise to a mass of tissue which consists of most cell types present in the larval nervous system and a number of other unidentified cell types. It too can be subculturedin vivo for many transfer generations.

The relative infrequency of neoplasms in insects is analyzed and an attempt is made to explain this infrequency and the occurrence of neoplasms in specific tissues of insects at specific developmental stages. Genetic and epigenetic neoplasms ofDrosophila are compared with neoplasms of other insects and of vertebrates and it is concluded that both genetic and epigenetic neoplasms ofDrosophila share the essential features of vertebrate neoplasms.

Zusammenfassung

In drei letalenDrosophila melanogaster-Mutanten wurde die Entwicklungspotenz von Neoplasmen untersucht und mit der Entwicklungspotenz der entsprechenden Wildtyp-Organe verglichen. Zwei dieser Neoplasmen wurden in den spätlarval-letalen, allelen Mutantenlethal (2) giant larvae 4 (l(2)gl 4) undlethal (2) giant larvae (l(2)gl) gefunden. Das dritte Neoplasma kommt in den letalen, hemizygoten, männlichen Embryonen der MutanteNotch 8 (Df(1)N 8) vor. Die Mutantel(2)gl 4 bzw. ihr Allell(2)gl, zeigen Schäden in den imaginalen Primordien ektodermaler Herkunft, so z.B. in den Imaginalscheiben des adulten Integuments und in den imaginalen optischen Primordien im larvalen Gehirn.l(2)gl 4 undl(2)gl besitzen zusätzlich noch vergrößerte Lymphdrüsen und abnormale Gonaden, Speichel- und Ringdrüsen. Sie transformieren die Imaginalscheiben zu benignen, letalen Neoplasmen und die imaginalen optischen Primordien im larvalen Gehirn zu einem malignen und letalen Neuroblastom. Beide Neoplasmen wurdenin vivo über viele Jahre in Abdomen adulter Weibchen gezüchtet, wo sie den Wirt binnen 7–14 Tage töteten. Die neoplastische Entwicklungsweise derl(2)gl 4 Imaginalscheiben als auch desl(2)gl 4 Gehirns erwies sich bei allen untersuchten Entwicklungsstadien (vom 10 Std alten Embryo bis zur erwachsenen Larve) als autonom. Im Metamorphosetest erfolgte keinerlei Differenzierung. Es wurde jedoch beobachtet, daß unter dem Einfluß der Metamorphosehormone die Zellen des Implantats sich nicht mehr teilten. Die Teilungsunfähigkeit blieb auch nach Abklingen der hormonalen Wirkung erhalten. Eine Ausnahme macht dasl(2)gl 4 Neuroblastom nach längerer Kulturin vivo. Diese Neuroblasten wachsen auch noch weiter, nachdem der hormonelle Einfluß erloschen ist. Sie töten den Wirt kurz nach dem Schlupfen oder bereits im Puppen-Stadium. Nach längerer Kulturin vivo zeigen vielel(2)gl 4 Neuroblasten abnormale Karyotypen und Zellgrößen.

Dasl(2)gl 4 Imaginalscheiben-Epithel ähnelt in Aufbau und Verhalten Gewebe-Sublinien, die aus Wildtyp-Imaginalscheiben nach Kulturin vivo hervorgehen. Offenbar hat der epigenetische Transformationsprozeß bei denl(2)gl 4 Imaginalscheiben.

Die Analyse einiger anderer spätlarvaler, letaler Mutanten, wiel(2)gd undl(1)d.lg.-1, die abnormale Imaginalscheiben besitzen, zeigte, daß sie auch Defekte in den imaginalen optischen Primordien im larvalen Gehirn verursachen.

Das Neoplasma im hemizygoten, männlichen Embryo der embryonal-letalen MutanteNotch 8 (Df(1)N 8), stellt eine Teratoma-ähnliche Wucherung dar, welche aus fast allen Zelltypen des larvalen Nervensystems, zusammengesetzt ist. In Abdomen adulter Weibchen implantiert verhalten sich diese Zellen maligne und letal.

Das relativ seltene Auftreten von Neoplasmen in Insekten wird diskutiert. Es wird versucht, das Vorkommen von Neoplasmen in bestimmten Insektengeweben mit den Eigenheiten der Insektenentwicklung zu korrelieren. Genetische und epigenetische Neoplasmen beiDrosophila werden mit Neoplasmen anderer Insekten und Vertebraten-Neoplasmen verglichen.

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Authors and Affiliations

  1. Center for Pathobiology, University of California, Irvine, 92664, Irvine, California, USA

    E. Gateff & Howard A. Schneiderman

  2. Biologisches Institut I (Zoologie) der Albert-Ludwigs-Universität, 78 Freiburg im Breisgau, Schanzlestraße 9, Federal Republic of Germany

    E. Gateff

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  1. E. Gateff
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  2. Howard A. Schneiderman
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Additional information

This work was supported in part by Grant CA 12643 from the National Institutes of Health. We thank Professor E. B. Lewis for mappingl(2)gl 4 and Drs. Peter Bryant and Clifton Poodry for thoughtful comments on the typescript.

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Gateff, E., Schneiderman, H.A. Developmental capacities of benign and malignant neoplasms ofDrosophila . W. Roux' Archiv f. Entwicklungsmechanik 176, 23–65 (1974). https://doi.org/10.1007/BF00577830

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