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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Aggarwal, S. K., King, R. C.: A comparative study of the ring gland from wild-type andl(2)gl mutantDrosophila melanogaster. J. Morph.129, 171–199 (1969)
Akai, H., Gateff, E., Schneiderman, H. A.: Virus-like particles in normal and tumorous tissues ofDrosophila. Science157, 810–813 (1967)
Bairati, A., Jr.: L'ultrastruttura dell'organo dell'emolinfa nella'larva diDrosophila melanogaster. Z. Zellforsch.61, 769–802 (1964)
Barigozzi, C.: Melanotic tumors inDrosophila. J. cell. comp. Physiol.52, 371–381 (1958)
Becker, H. J.: Über Röntgenmosaikflecken und Defektmutationen am Auge vonDrosophila und die Entwicklungsphysiologie des Auges. Z. inunkt. Abstamm.-u. Vererb.-L.88, 333–373 (1957)
Becker, H. J.: Die Puffs von Speicheldrüsenchromosomen vonDrosophila melanogaster. I. Beobachtungen zum Verhalten des Puffmusters im Normalstamm und bei zwei Mutanten, Giant und Lethal-giant-Larvae. Chromosoma (Berl.)10, 651–678 (1959)
Bernard, W., Granboulan, N.: The fine structure of the cancer cell nucleus. Exp. Cell Res., Suppl.9, 19–53 (1963)
Bodenstein, D.: The postembryonic development ofDrosophila. In: M. Demerec, Biology of Drosophila. New York: Hafner 1950
Braun, A. C.: Understanding the cancer problem. New York: Columbia University Press 1969
Bryant, P. J.:l(2)gd: lethal (2)giant disc. Drosoph. Inf. Serv.44, 47 (1969)
Bryant, P. J., Schneiderman, H. A.: Cell lineage, growth and determination in the imaginal leg disc ofDrosophila melanogaster. Develop. Biol.20, 263–290 (1969)
Bryant, P. J., Schubiger, G.: Giant and duplicated imaginal discs in a new lethal mutant ofDrosophila melanogaster. Develop. Biol.24, 233–263 (1971)
Chen, P. S.: A comparative study of the oxygen consumption in the three lethal mutants “ltr,”“lgl,” and “lme” ofDrosophila melanogaster. Z. indukt. Abstamm.-u. Vererb.-L.84, 38–70 (1951)
Chevais, S.: Determinisme de la taille de l'oeil chez le mutant Bar de laDrosophile. Bull. biol. Fr. Belg.78, 71–110 (1944)
Counce, S. J.: Studies on female-sterility genes inDrosophila melanogaster. I. The effects of the genedeep orange on embryonic development. Z. indukt. Abstamm.-u. Vererb.-L.87, 443–461 (1956a)
Counce, S. J.: Studies on female sterility genes inDrosophila melanogaster. II. The effects of the genefused on embryonic development. Z. indukt. Abstamm.-u. Vererb.-L.87, 462–481 (1956b)
Counce, S. J.: Studies on female sterility genes inDrosophila melanogaster. III. The effects of the generudimentary on embryonic development. Z. indukt. Abstamm.-u. Vererb.-L.87, 482–492 (1956c)
Counce, S. J.: The causal analysis of insect embryogenesis. In: S. Counce and C. H. Waddington, Developmental systems: insects, vol. 2, p. 1–156. New York: Academic Press 1973
Cowdry, E. V.: Cancer cells. Philadelphia: W. B. Saunders 1955
Ede, D. A.: Studies on the lethal effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. I. A preliminary survey of some sex-linked lethal stocks and an analysis of the mutantLff 11. Wilhelm Roux' Arch. Entwickl.-Mech. Org.148, 416–436 (1956a)
Ede, D. A.: Studies on the lethal effects of some genetic lethal factors of the embryonic development ofDrosophila melanogaster. II. An analysis of the mutant X-2. Wilhelm Roux' Arch. Entwickl.-Mech. Org.148, 437–451 (1956b)
Ede, D. A.: Studies on the effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. III. An analysis of the mutant X-27. Wilhelm Roux' Arch. Entwickl.-Mech. Org.149, 88–100 (1956c)
Ede, D. A.: Studies on the effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. IV. An analysis of the mutant X-20. Wilhelm Roux' Arch. Entwickl.-Mech. Org.149, 101–144 (1956d)
Ede, D. A.: Studies on the effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. V. An analysis of the mutant X-10. Wilhelm Roux' Arch. Entwickl.-Mech. Org.149, 247–258 (1956e)
Ede, D. A.: Studies on the effects of some genetic lethal factors on the embryonic development ofDrosophila melanogaster. VI. An analysis of the mutant S9. Wilhelm Roux' Arch. Entwickl.-Mech. Org.149, 402–415 (1956f)
Edwards, J. S., Kobal, J., Rudy, G.: Pathological changes following salivary duct ligation in cockroaches. J. Invert. Path.9, 160–163 (1967)
Engel, C. S.: Warum erkranken wirbellose Tiere nicht an Krebs. Z. Krebsforsch.82, 531–543 (1930)
Faulhaber, T.: Biochemische Untersuchungen zum Eiweiß-Stoffwechsel der Letalmutante “lethal giant larvae” (lgl) vonDrosophila melanogaster. Z. Vererb.-L.90, 299–334 (1959)
Federley, H.: Sex limited hereditary cancer in lepidopterous larvae. Hereditas (Lund)22, 193–216 (1936)
Fraser-Rowell, C. H.: A general method for silvering invertebrate central nervous systems. Quart. J. micr. Sci.104, 81–87 (1963)
Garcia-Bellido, A.: Larvalentwicklung transplantierter Organe vonDrosophila melanogaster im Adultmilieu. J. Insect Physiol.11, 1071–1078 (1965)
Garcia-Bellido, A., Merriam, J. R.: Cell lineage of the imaginal discs inDrosophila gynandromorphs. J. exp. Zool.170, 61–75 (1969)
Gardner, E. J.: Tumorous head inDrosophila. Advanc. Genet.15, 116–146 (1970)
Gateff, E.: Developmental and histological studies of wild-type and mutant tissues ofDrosophila melanogaster. Ph. D. Thesis, Univ. Calif., Irvine 1971
Gateff, E., Schneiderman, H. A.: Developmental studies of a new mutant ofDrosophila melanogaster: lethal malignant brain tumor (l(2)gl4) (Abstract 218). Amer. Zool.7, 760
Gateff, E., Schneiderman, H. A.: Neoplasms in mutant and cultured wild-type tissues ofDrosophila. Nat. Cancer Inst. Monogr.31, 365–397 (1969a)
Gateff, E., Schneiderman, H. A.:l(2)gl 4:lethal (2) giant larva4. Drosoph. Inf. Serv.44, 47–48 (1969b)
Gateff, E., Schneiderman, H. A.: Developmental capacities of immature eye-antennal imaginal discs ofDrosophila. Wilhelm Roux' Arch. Entwickl.-Mech. Org. (In press)
Gateff, E., Akai, H., Schneiderman, H. A.: Developmental, histological and fine structure studies on tissue sublines derived from the eye-antennal imaginal disc ofDrosophila melanogaster inin vivo culture. Wilhelm Roux' Arch. Entwickl.-Mech. Org. (In press)
Gehring, W., Nothiger, R.: The imaginal discs ofDrosophila. In: S. Counce and C. H. Waddington, Developmental systems: Insects, vol. 2, p. 211–290. New York: Academic Press 1973
Gloor, H.: Entwicklungsphysiologische Untersuchungen an den Gonaden der Letalrasse (lgl) vonDrosophila melanogaster. Rev. suisse Zool.50, 339–393 (1943)
Grob, H.: Entwicklungsphysiologische Untersuchungen an den Speicheldrüsen, dem Darmtraktus und den Imaginalscheiben einer Letalrasse (lgl) vonDrosophila melanogaster. Z. indukt. Abstamm.-u. Vererb.-L.84, 320–360 (1952)
Gross, L.: Oncogenic viruses. New York: Pergamon Press 1970
Hadorn, E.: An accelerating effect of normal “ring glands” on puparium formation in lethal larvae ofDrosophila melanogaster. Proc. nat. Acad. Sci. (Wash.)23, 478–484 (1937a)
Hadorn, E.: Transplantation of gonads from lethal to normal larvae ofDrosophila melanogaster. Proc. Soc. exp. Biol. (N.Y.)36, 632–634 (1937b)
Hadorn, E.: Hormonale Kontrolle der Pupariumbildung bei Fliegen. Naturwissenschaften42, 681–682 (1937c)
Hadorn, E.: Die Degeneration der Imaginalscheiben bei letalenDrosophila Larven der Mutation “letal giant.” Rev. suisse Zool.46, 425–429 (1938)
Hadorn, E.: Gene action in growth and differentiation of lethal mutants ofDrosophila. Symp. Soc. exp. Biol.2 (1948)
Hadorn, E.: Differenzierungsleistungen wiederholt fragmentierter Teilstücke männlicher Genitalscheiben vonDrosophila melanogaster nach Kulturin vivo. Develop. Biol.7, 617–629 (1963)
Hadorn, E.: Konstanz, Wechsel und Typus der Determination und Differenzierung in Zellen aus männlichen Genitalscheiben vonDrosophila melanogaster in Dauerkultur. Develop. Biol.13, 424–509 (1966)
Hadorn, E.: Proliferation and dynamics of cell heredity in blastema cultures ofDrosophila Nat. Cancer Inst. Monogr.31, 351–364 (1969)
Hadorn, E., Garcia-Bellido, A.: Zur Proliferation vonDrosophila Zellkulturen im Adultmilieu. Rev. suisse Zool.71, 576–582 (1964)
Hadorn, E., Gloor, H.: Die Auswirkung eines Letalfaktors (lgl) beiDrosophila melanogaster auf Wachstum und Differenzierung der Gonaden. Rev. suisse Zool.49, 228–236 (1942)
Hadorn, E., Neel, J.: Der hormonale Einfluß der Ringdrüse (Corpus allatum) auf die Pupariumbildung bei Fliegen. Wilhelm Roux' Arch. Entwickl.-Mech. Org.138, 281–304 (1938)
Hadorn, E., Hurlimann, R., Mindek, G., Schubiger, G., Staub, M.: Entwicklungsleistungen embryonaler Blasteme vonDrosophila nach Kultur im Adultwirt. Rev. suisse Zool.75, 558–567 (1968)
Harshbarger, J. C., Taylor, R. L.: Neoplasms in insects. A. Rev. Ent.13, 159–190 (1968)
Hotta, Y., Benzer, S.: Mapping of behaviour inDrosophila mosaics. Nature (Lond.)240, 527–535 (1972)
Johansson, A. S., Schreiner, B.: Intestinal tumors in the German cockroachBlatella germanica L. Nature (Lond.)212, 845 (1966)
Juniper, K., Chester, C. L.: A filter membrane technique for cytological study of exfoliated cells in body fluids. Cancer (Philad.)12, 278–285 (1959)
Karlson, P., Hanser, G.: Über die Wirkung des Puparisierungshormons bei der Wildform und der Mutantelgl vonDrosophila. Z. Naturforsch.7, 80–83 (1952)
King, R. C.: Ovarian development inDrosophila melanogaster. New York and London: Academic Press 1970
King, R. C., Burnett, R. G., Staley, N. A.: Oogenesis in adultDrosophila melanogaster. IV. Heredity ovarian tumors. Growth21, 239–261 (1957)
Kopriwa, B., Leblond, C. P.: Improvement of the coating technique of autoradiography. J. Histochem. Cytochem.10, 269–286 (1962)
Krishnakumaran, A., Berry, S. J., Oberlander, H., Schneiderman, H. A.: Nucleic acid synthesis during insect development. II. Control of DNA synthesis in the Cecropia silkworm and other saturniid moths. J. Insect Physiol.13, 1–57 (1967)
Krishnakumaran, A., Schneiderman, H. A.: Developmental capacities of the cells of an adult moth. J. exp. Zool.157, 293–305 (1964)
Levan, A.: Relation of chromosome studies to the origin and progression of tumors: The evidence of chromosome numbers. In: Genetics and cancer, a collection of papers. Symp. Fund. Cancer Res., 13th, p. 151–182. Anderson Hospital and Tumor Institute, Austin, Texas 1959
Lindsley, D. L., Grell, E. H.: Genetic variations ofDrosophila melanogaster. Carnegie Inst. Wash. Publ. No. 627 (1968)
Little, C. C.: The genetics of cancer in mice. Biol. Rev.22, 315–348 (1947)
Loewenstein, W. R.: Membrane junctions in growth and differentiation. Fed. Proc.32, 60–64 (1973)
Markert, C. L., Ursprung, H.: Abnormal development and cancer. In: Developmental genetics, p. 194–202. New York: Prentice-Hall 1971
Matz, G.: Tumours experimentales chezLeucophaea maderae Fabr. etLocusta migratoria L. J. Insect Physiol.6, 309–313 (1961)
Matz, G., Weil, J.-H., Joly, P., Ebel, J.-P.: Transmission of tumors inLocusta migratoria Linnaeus by nucleic acid extracted from the tumors. J. Invert. Path.8, 8–13 (1966)
Melander, Y., Wingstrand, K. G.: Gomori's hematoxylin as a chromosome stain. Stain Technol.28, 217–223 (1953)
Mindek, G.: Metamorphosis of imaginal discs ofDrosophila melanogaster. Wilhelm Roux' Archiv169, 353–356 (1972)
Mohr, O. L.: Character changes caused by mutation of an entire region of a chromosome inDrosophila. Genetics4, 275–282 (1919)
Nayar, K. K., Arthur, E., Balls, M.: The transmission of tumours induced in cockroaches by nerve severance. Experientia (Basel)27, 183 (1971)
Oberlander, H.: The hormonal control of development of imaginal disks. In: H. Ursprung and R. Nothiger, Results and problems in cell differentiation, vol. 5, p. 155–172. Berlin-Heidelberg-New York: Springer 1972
Oftedal, P.: The histogenesis of a new tumor inDrosophila melanogaster, and a comparison with tumors of five other stocks. Z. indukt. Abstamm.-u. Vererb.-L.85, 408–422 (1953)
Oster, I. I., Balaban, G.: A modified method for preparing somatic chromosomes. Drosoph. Inf. Serv.37, 142–144 (1963)
Poodry, C. A., Schneiderman, H. A.: The ultrastructure of the developing leg ofDrosophila melanogaster. Wilhelm Roux' Archiv166, 1–44 (1970)
Postlethwait, J. H., Schubiger, G., Bryant, P. J.: The homoeotic effect of “tumorous head” inDrosophila melanogaster, Develop. Biol.29, 337–342 (1972)
Poulson, D. F.: The effect of certain X-chromosome deficiencies on the embryonic development ofDrosophila melanogaster. J. exp. Zool.83, 271–325 (1940)
Poulson, D. F.: Histogenesis, organogenesis and differentiation in the embryo ofDrosophila melanogaster. In: M. Demerec, Biology ofDrosophila, p. 209–244. New York: Hafner 1950
Remensberger, P.: Cytologische und histologische Untersuchungen an Zellstämmen vonDrosophila melanogaster nach Dauerkulturin vivo. Chromosoma (Berl.)23, 386–417 (1968)
Satir, P., Gilula, N. B.: The fine structure of membranes and intercellular communication in insects. A. Rev. Ent.18, 143–166 (1973)
Scharrer, B.: Experimental tumors after nerve section in an insect. Proc. Soc. exp. Biol. (N.Y.)60, 184–189 (1945)
Scharrer, B., Hadorn, E.: The structure of the ring gland (corpus allatum) in normal and lethal larvae ofDrosophila melanogaster. Proc. nat. Acad. Sci. (Wash.)24, 236–242 (1938)
Schnitter, M.: Zur Genetik und Entwicklungsphysiologie des Faktors “letal Scheiben defekt” (lsd) beiDrosophila melanogaster. Rev. suisse Zool.68, 345–418 (1961)
Scriba, M. E. L.: Beeinflussung der frühen Embryonalentwicklung vonDrosophila melanogaster durch Chromosomenaberrationen. Zool. Jb. (Anat.)81, 435–490 (1964)
Scriba, M. E. L.: Embryonale Entwicklungsstörungen bei Defizienz und Tetraploidie des 2 Chromosoms vonDrosophila melanogaster. Wilhelm Roux' Arch. Entwickl.-Mech. Org.159, 314–345 (1967)
Scriba, M. E. L.: Embryonale Entwicklungsstörungen bei Nullosomie und Tetrasomie des 3 Chromosoms vonDrosophila melanogaster. Develop. Biol.19, 160–171 (1969)
Seiler, J., Puchta, O.: Die Fortpflanzungsbiologie derSolenobien (Lepid. Psychidae): Verhalten bei Artkreuzungen und F1 Resultate. Wilhelm Roux' Arch. Entwickl.-Mech. Org.149, 115–137 (1956)
Shatoury, H. H. El: The structure of the lymph glands ofDrosophila larvae. Wilhelm Roux' Arch. Entwickl.-Mech. Org.147, 489–495 (1955a)
Shatoury, H. H. El: A genetically controlled malignant tumour inDrosophila. Wilhelm Roux' Arch. Entwickl.-Mech. Org.147, 496–522 (1955b)
Shatoury, H. H. El., Waddington, C. H.: Function of the lymph gland cells during the larval period. J. Embryol. exp. Morph.5, 123–133 (1957)
Slizynska, H.: Salivary chromosome analysis of the white-facet region ofDrosophila melanogaster. Genetics23, 291–299 (1938)
Stewart, M., Murphy, C., Fristrom, J.: The recovery and preliminary characterization of X chromosome mutants affecting imaginal discs ofDrosophila melanogaster. Develop. Biol.27, 71–83 (1972)
Sutherland, D. J.: Experimentally induced tumors inPeriplaneta americana (L.). J. Insect Physiol.9, 131–135 (1963)
Sutherland, D. J.: The development of salivary tumors inPeriplaneta americana (L.) as induced by duct ligation. J. Insect Physiol.13, 137–152 (1967)
Teutschlander, O.: Beiträge zur vergleichenden Onkologie mit Berücksichtigung der Identitätsfrage. Z. Krebsforsch.17, 283–407 (1920)
Tjio, J. H., Puck, T. T.: Genetics of somatic mammalian cells: II. Chromosome constitution of cells in tissue culture. J. exp. Med.108, 259–268 (1958)
Tobler, H.: Zellspezifische Determination und Beziehung zwischen Proliferation und Transdetermination in Bein- und Flügelprimordien vonDrosophila melanogaster. J. Embryol. exp. Morph.16, 609–633 (1966)
Ursprung, H.: The fine structure of imaginal disks. In: H. Ursprung and R. Nothiger, Results and problems in cell differentiation, vol. 5, p. 93–107. Berlin-Heidelberg-New York: Springer 1972
Vogt, M.: Verhalten transplantierter Ringdrüsen „letaler“Drosophila larven. Z. Naturforsch.2, 292–294 (1947)
Welch, R. M.: A developmental analysis of the lethal mutantl(2)gl ofDrosophila melanogaster based on cytophotometric determination of nuclear desoxyribonucleic acid (DNA) content. Genetics42, 544 (1957)
Welch, R. M., Resch, K.: A cytologieal analysis of DNA and protein in salivary gland and gut of the lethal mutantlgl ofDrosophila melanogaster. Int. Congr. Genet., 11th (1963)
Willis, R. A.: Pathology of tumors. London: Butterworth and Co. 1948
Wright, T. R. F.: The genetics of embryogenesis inDrosophila. Advanc. Genet.15, 261–395 (1970)
Author information
Authors and Affiliations
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.
Rights and permissions
About this article
Cite this article
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
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00577830