Advertisement

Chromosome Research

, Volume 25, Issue 3–4, pp 201–214 | Cite as

Polyteny: still a giant player in chromosome research

  • Benjamin M. Stormo
  • Donald T. FoxEmail author
Waldeyer-Flemming Special Collection

Abstract

In this era of high-resolution mapping of chromosome territories, topological interactions, and chromatin states, it is increasingly appreciated that the positioning of chromosomes and their interactions within the nucleus is critical for cellular function. Due to their large size and distinctive structure, polytene chromosomes have contributed a wealth of knowledge regarding chromosome regulation. In this review, we discuss the diversity of polytene chromosomes in nature and in disease, examine the recurring structural features of polytene chromosomes in terms of what they reveal about chromosome biology, and discuss recent advances regarding how polytene chromosomes are assembled and disassembled. After over 130 years of study, these giant chromosomes are still powerful tools to understand chromosome biology.

Keywords

Polytene Polyploid Endocycle 

Abbreviations

TGC

Trophoblast giant cell

TAD

Topologically associated domain

TEV

Tobacco etch virus

Su(UR)

Suppressor of under-replication

References

  1. Aggarwal BD, Calvi BR (2004) Chromatin regulates origin activity in drosophila follicle cells. Nature 430(6997):372–376PubMedCrossRefGoogle Scholar
  2. Alexander JL, Barrasa MI, Orr-Weaver TL (2015) Replication fork progression during re-replication requires the DNA damage checkpoint and double-strand break repair. Curr Biol 25(12):1654–1660PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ammermann D (1971) Morphology and development of the macronuclei of the ciliates Stylonychia Mytilus and Euplotes Aediculatus. Chromosoma 33(2):209–238PubMedCrossRefGoogle Scholar
  4. Ammermann D (1987) Giant Chromosomes in Ciliates. In: Hennig W (ed) Structure and Function of Eukaryotic Chromosomes. Springer Berlin Heidelberg, Berlin, pp 59–67CrossRefGoogle Scholar
  5. Ammermann D et al (1974) The development of the macronucleus in the ciliated protozoan Stylonychia Mytilus. Chromosoma 45(4):401–429PubMedCrossRefGoogle Scholar
  6. Andreyeva EN et al (2008) Local DNA underreplication correlates with accumulation of phosphorylated H2Av in the Drosophila Melanogaster polytene chromosomes. Chromosom Res 16(6):851–862CrossRefGoogle Scholar
  7. Ashburner M (1980) Some Aspects of the Structure and Function of the Polytene Chromosomes of Diptera. In: Blackman RL, Hewitt GM, Ashburner M (eds) Insect cytogenetics. Blackwell, Oxford, pp 65–84Google Scholar
  8. Ashburner M, Bonner JJ (1979) The induction of gene activity in drosophila by heat shock. Cell 17(2):241–254PubMedCrossRefGoogle Scholar
  9. Balbiani E (1881) Sur la structure du noyau des cellules salivaires chez les larves de Chironomus. Zool Anz 4(637–641):662–667Google Scholar
  10. Balbiani E (1890) Sur la structure intime du noyau du Loxophyllum meleagris. Zool Anz 13(110–115):132–136Google Scholar
  11. Barlow PW, Sherman MI (1974) Cytological studies on the organization of DNA in giant trophoblast nuclei of the mouse and the rat. Chromosoma 47(2):119–131PubMedCrossRefGoogle Scholar
  12. Bauer CR, Hartl TA, Bosco G (2012) Condensin II promotes the formation of chromosome territories by inducing axial compaction of Polyploid interphase chromosomes. PLoS Genet 8(8):e1002873PubMedPubMedCentralCrossRefGoogle Scholar
  13. Belyaeva ES et al (1998) Su(UR)ES: a gene suppressing DNA underreplication in intercalary and pericentric heterochromatin of Drosophila Melanogaster polytene chromosomes. Proc Natl Acad Sci U S A 95(13):7532–7537PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bender W, Spierer P, Hogness DS (1983) Chromosomal walking and jumping to isolate DNA from the ace and rosy loci and the bithorax complex in Drosophila Melanogaster. J Mol Biol 168(1):17–33PubMedCrossRefGoogle Scholar
  15. Biesele J, Poyner H (1943) Polytene chromosomes in two mammary carcinomas of the human subject. Cancer Res 3:779–783Google Scholar
  16. Blakeslee AF, Avery AG (1937) Methods of inducing doubling of chromosomes in plants by treatment with colchicine*. J Hered 28(12):393–411CrossRefGoogle Scholar
  17. Bostock CJ, Prescott DM (1972) Evidence of gene diminution during the formation of the macronucleus in the protozoan, Stylonychia (DNA density-melting curves-micronuclear DNA-polytene chromosomes). Proc Natl Acad Sci 69(1):139–142PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bower DJ (1987) Chromosome organisation in polyploid mouse trophoblast nuclei. Chromosoma 95(1):76–80PubMedCrossRefGoogle Scholar
  19. Bretscher HS, Fox DT (2016) Proliferation of double-strand break-resistant Polyploid cells requires drosophila FANCD2. Dev Cell 37(5):444–457PubMedPubMedCentralCrossRefGoogle Scholar
  20. Breuer ME, Pavan C (1955) Behavior of polytene chromosomes of Rhynchosciara Angelae at different stages of larval development. Chromosoma 7(1):371–386CrossRefGoogle Scholar
  21. Calvi BR (2013) Making big cells: one size does not fit all. Proc Natl Acad Sci 110(24):9621–9622PubMedPubMedCentralCrossRefGoogle Scholar
  22. Calvi BR, Spradling AC (2001) The nuclear location and chromatin organization of active chorion amplification origins. Chromosoma 110(3):159–172PubMedCrossRefGoogle Scholar
  23. Calvi BR, Lilly MA, Spradling AC (1998) Cell cycle control of chorion gene amplification. Genes Dev 12(5):734–744PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cantero G et al (2006) Topoisomerase II inhibition and high yield of endoreduplication induced by the flavonoids luteolin and quercetin. Mutagenesis 21(5):321–325PubMedCrossRefGoogle Scholar
  25. Carvalheira GMG (2000) Plant polytene chromosomes. Genet Mol Biol 23:1043–1050CrossRefGoogle Scholar
  26. Chalker DL, Yao MC (2011) DNA elimination in ciliates: transposon domestication and genome surveillance. Annu Rev Genet 45:227–246PubMedCrossRefGoogle Scholar
  27. Cross JC (2014) More of a good thing or less of a bad thing: gene copy number variation in Polyploid cells of the placenta. PLoS Genet 10(5):e1004330PubMedPubMedCentralCrossRefGoogle Scholar
  28. Davoli T, de Lange T (2012) Telomere-driven Tetraploidization occurs in human cells undergoing crisis and promotes transformation of mouse cells. Cancer Cell 21(6):765–776PubMedPubMedCentralCrossRefGoogle Scholar
  29. Davoli T, Denchi EL, de Lange T (2010) Persistent telomere damage induces bypass of mitosis and tetraploidy. Cell 141(1):81–93PubMedPubMedCentralCrossRefGoogle Scholar
  30. Dej KJ, Spradling AC (1999) The endocycle controls nurse cell polytene chromosome structure during drosophila oogenesis. Development 126(2):293–303PubMedGoogle Scholar
  31. Delidakis C, Kafatos FC (1989) Amplification enhancers and replication origins in the autosomal chorion gene cluster of drosophila. EMBO J 8(3):891–901PubMedPubMedCentralGoogle Scholar
  32. Diaz M, Pavan C (1965) Changes in chromosomes induced by microorganism infection. Proc Natl Acad Sci 54(5):1321–1327PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dorsett D et al (2005) Effects of sister chromatid cohesion proteins on cut gene expression during wing development in drosophila. Development 132(21):4743–4753PubMedPubMedCentralCrossRefGoogle Scholar
  34. Eagen KP, Hartl TA, Kornberg RD (2015) Stable chromosome condensation revealed by chromosome conformation capture. Cell 163(4):934–946PubMedPubMedCentralCrossRefGoogle Scholar
  35. Endow SA, Gall JG (1975) Differential replication of satellite DNA in polyploid tissues of Drosophila Virilis. Chromosoma 50(2):175–179PubMedCrossRefGoogle Scholar
  36. Erenpreisa J et al (2009) The role of meiotic cohesin REC8 in chromosome segregation in γ irradiation-induced endopolyploid tumour cells. Exp Cell Res 315(15):2593–2603PubMedCrossRefGoogle Scholar
  37. Ficq A, Pavan C (1957) Autoradiography of polytene chromosomes of Rhynchosciara Angelae at different stages of larval development. Nature 180(4593):983–984PubMedCrossRefGoogle Scholar
  38. Flemming W (1882) Zellsubstanz, kern und zelltheilung. Vogel, LiepzigGoogle Scholar
  39. Fox DT, Duronio RJ (2013) Endoreplication and polyploidy: insights into development and disease. Development 140(1):3–12PubMedPubMedCentralCrossRefGoogle Scholar
  40. Fox DT, Gall JG, Spradling AC (2010) Error-prone polyploid mitosis during normal drosophila development. Genes Dev 24(20):2294–2302PubMedPubMedCentralCrossRefGoogle Scholar
  41. Fragkos M et al (2015) DNA replication origin activation in space and time. Nat Rev Mol Cell Biol 16(6):360–374PubMedCrossRefGoogle Scholar
  42. Gelbart WM, Wu C-T (1982) Interactions of Zeste mutations with loci exhibiting Transvection effects in DROSOPHILA MELANOGASTER. Genetics 102(2):179–189PubMedPubMedCentralGoogle Scholar
  43. Glover DM et al (1982) Gene amplification in Rhynchosciara salivary gland chromosomes. Proc Natl Acad Sci 79(9):2947–2951PubMedPubMedCentralCrossRefGoogle Scholar
  44. Goodrich JS, Clouse KN, Schüpbach T (2004) Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in drosophila oogenesis. Development 131(9):1949PubMedCrossRefGoogle Scholar
  45. Hammond MP, Laird CD (1985a) Chromosome structure and DNA replication in nurse and follicle cells of Drosophila Melanogaster. Chromosoma 91(3–4):267–278PubMedCrossRefGoogle Scholar
  46. Hammond MP, Laird CD (1985b) Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila Melanogaster. Chromosoma 91(3):279–286PubMedCrossRefGoogle Scholar
  47. Hannibal RL, Baker JC (2016) Selective amplification of the genome surrounding key placental genes in trophoblast Giant cells. Curr Biol 26(2):230–236PubMedCrossRefGoogle Scholar
  48. Hannibal RL et al (2014) Copy number variation is a fundamental aspect of the placental genome. PLoS Genet 10(5):e1004290PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hartl TA, Smith HF, Bosco G (2008) Chromosome alignment and Transvection are antagonized by Condensin II. Science 322(5906):1384–1387PubMedCrossRefGoogle Scholar
  50. Heitz E (1933) Die somatische Heteropyknose bei Drosophila melanogaster und ihre genetische Bedeutung. Z Zellforsch Mikrosk Anat 20(1):237–287CrossRefGoogle Scholar
  51. Holm C et al (1985) DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41(2):553–563PubMedCrossRefGoogle Scholar
  52. Hook SS, Lin JJ, Dutta A (2007) Mechanisms to control Rereplication and implications for cancer. Curr Opin Cell Biol 19(6):663–671PubMedPubMedCentralCrossRefGoogle Scholar
  53. Ilyinskaya NB (1994) Seasonal changes in the polytene chromosomes of Chironomidae. Tsitologia 36(7):605–622Google Scholar
  54. Keyes LN, Spradling AC (1997) The drosophila gene fs(2)cup interacts with otu to define a cytoplasmic pathway required for the structure and function of germ-line chromosomes. Development 124(7):1419–1431PubMedGoogle Scholar
  55. Kim JC et al (2011) Integrative analysis of gene amplification in drosophila follicle cells: parameters of origin activation and repression. Genes Dev 25(13):1384–1398PubMedPubMedCentralCrossRefGoogle Scholar
  56. King R et al (1981) Giant polytene chromosomes from the ovaries of a drosophila mutant. Science 212(4493):441–443PubMedCrossRefGoogle Scholar
  57. Kloetzel JA (1970) Compartmentalization of the developing macronucleus following conjugation in Stylonychia Euplotes. J Cell Biol 47(2):395PubMedPubMedCentralCrossRefGoogle Scholar
  58. Klusza S, Deng W-M (2010) Poly is required for nurse cell chromosome dispersal and oocyte polarity in drosophila. Fly 4(2):128–136PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kokkinos MI et al (2010) Cadherins in the human placenta--epithelial-mesenchymal transition (EMT) and placental development. Placenta 31(9):747–755PubMedCrossRefGoogle Scholar
  60. Landis G et al (1997) The k43 gene, required for chorion gene amplification and diploid cell chromosome replication, encodes the drosophila homolog of yeast origin recognition complex subunit 2. Proc Natl Acad Sci 94(8):3888–3892PubMedPubMedCentralCrossRefGoogle Scholar
  61. Letsou A, Bohmann D (2005) Small flies—big discoveries: nearly a century of drosophila genetics and development. Dev Dyn 232(3):526–528PubMedCrossRefGoogle Scholar
  62. Levan A (1938) The effect of colchicine on root mitoses in allium. Hereditas 24(4):471–486CrossRefGoogle Scholar
  63. Levan A (1939) Tetraploidy and Octoploidy induced by colchicine in diploid petunia. Hereditas 25(2):109–131CrossRefGoogle Scholar
  64. Levan A, Hauschka TS (1953) Endomitotic reduplication mechanisms in ascites tumors of the mouse. J Natl Cancer Inst 14(1):1–43PubMedGoogle Scholar
  65. Liao WX et al (2012) Human placental expression of SLIT/ROBO signaling cues: effects of preeclampsia and hypoxia. Biol Reprod 86(4):111PubMedPubMedCentralCrossRefGoogle Scholar
  66. Mahowald AP, Strassheim JM (1970) Intercellular migration of centrioles in the Germarium of Drosophila Melanogaster. J Cell Biol 45(2):306PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mahowald AP et al (1979) Loss of centrioles and polyploidization in follicle cells of Drosophila Melanogaster. Exp Cell Res 118(2):404–410PubMedCrossRefGoogle Scholar
  68. Maqbool SB et al (2010) Dampened activity of E2F1-DP and Myb-MuvB transcription factors in drosophila endocycling cells. J Cell Sci 123(Pt 23):4095–4106PubMedPubMedCentralCrossRefGoogle Scholar
  69. Markov AV et al (2003) Localization of cohesin complexes of polytene chromosomes of Drosophila Melanogaster located on interbands. Genetika 39(9):1203–1211PubMedGoogle Scholar
  70. Marks GE, Davies DR (1979) The cytology of cotyledon cells and the induction of giant polytene chromosomes inPisum sativum. Protoplasma 101(1):73–80CrossRefGoogle Scholar
  71. Mehrotra S et al (2008) Endocycling cells do not apoptose in response to DNA rereplication genotoxic stress. Genes Dev 22(22):3158–3171PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mellert DJ, Truman JW (2012) Transvection is common throughout the drosophila genome. Genetics 191(4):1129–1141PubMedPubMedCentralCrossRefGoogle Scholar
  73. Metz CW (1916) Chromosome studies on the Diptera. II. The paired association of chromosomes in the Diptera, and its significance. J Exp Zool 21(2):213–279CrossRefGoogle Scholar
  74. Meyer GF, Lipps HJ (1980) Chromatin elimination in the hypotrichous ciliate Stylonychia Mytilus. Chromosoma 77(3):285–297PubMedCrossRefGoogle Scholar
  75. Meyer GF, Lipps HJ (1981) The formation of polytene chromosomes during macronuclear development of the hypotrichous ciliate Stylonychia Mytilus. Chromosoma 82(2):309–314PubMedCrossRefGoogle Scholar
  76. Murti KG, Prescott DM (1999) Telomeres of polytene chromosomes in a ciliated protozoan terminate in duplex DNA loops. Proc Natl Acad Sci U S A 96(25):14436–14439PubMedPubMedCentralCrossRefGoogle Scholar
  77. Nagl W (1969) Banded polytene chromosomes in the legume Phaseolus Vulgaris. Nature 221:70–71PubMedCrossRefGoogle Scholar
  78. Nagl W (1972) Giant sex chromatin in endopolyploid trophoblast nuclei of the rat. Experientia 28(2):217–218PubMedCrossRefGoogle Scholar
  79. Nagl W (1974) The Phaseolus suspensor and its polytene chromosomes. Z Pflanzenphysiol 73(1):1–44CrossRefGoogle Scholar
  80. Nagl W (1978) Endopolyploidy and polyteny in differentiation and evolution: towards an understanding of quantitative and qualitative variation of nuclear DNA in ontogeny and phylogeny. North-Holland Publishing Company, AmsterdamGoogle Scholar
  81. Nagl W (1981) Polytene chromosomes of plants. Int Rev Cytol 73:21–53CrossRefGoogle Scholar
  82. Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43(1):525–558PubMedCrossRefGoogle Scholar
  83. Nordman J, Orr-Weaver TL (2012) Regulation of DNA replication during development. Development 139(3):455–464PubMedPubMedCentralCrossRefGoogle Scholar
  84. Nordman J et al (2011) Developmental control of the DNA replication and transcription programs. Genome Res 21(2):175–181PubMedPubMedCentralCrossRefGoogle Scholar
  85. Ohno S, Kaplan WD, Kinosita R (1959) Formation of the sex chromatin by a single X-chromosome in liver cells of Rattus Norvegicus. Exp Cell Res 18(2):415–418PubMedCrossRefGoogle Scholar
  86. Orr-Weaver TL (2015) When bigger is better: the role of polyploidy in organogenesis. Trends Genet 31(6):307–315PubMedPubMedCentralCrossRefGoogle Scholar
  87. Orr-Weaver TL, Spradling AC (1986) Drosophila chorion gene amplification requires an upstream region regulating s18 transcription. Mol Cell Biol 6(12):4624–4633PubMedPubMedCentralCrossRefGoogle Scholar
  88. Osheim YN, Miller OL (1983) Novel amplification and transcriptional activity of chorion genes in Drosophila Melanogaster follicle cells. Cell 33(2):543–553PubMedCrossRefGoogle Scholar
  89. Painter TS (1933) A new method for the study of chromosome rearrangements and the plotting of chromosome maps. Science 78(2034):585–586PubMedCrossRefGoogle Scholar
  90. Pandit SK, Westendorp B, de Bruin A (2013) Physiological significance of polyploidization in mammalian cells. Trends Cell Biol 23(11):556–566PubMedCrossRefGoogle Scholar
  91. Pauli A et al (2008) Cell-type-specific TEV protease cleavage reveals Cohesin functions in drosophila neurons. Dev Cell 14(2):239–251PubMedPubMedCentralCrossRefGoogle Scholar
  92. Pauli A et al (2010) A direct role for Cohesin in gene regulation and ecdysone response in drosophila salivary glands. Curr Biol 20(20):1787–1798PubMedPubMedCentralCrossRefGoogle Scholar
  93. Pavan C, Breuer ME (1952) Polytene chromosomes in different tissues of Rhynchosciara. J Hered 43(4):151–158CrossRefGoogle Scholar
  94. Pavan C, da Cunha AB, Morsoletto C (1971) Virus-chromosome relationships in cells of Rhynchosciara (Diptera, Sciaridae). Caryologia 24(3):371–389CrossRefGoogle Scholar
  95. Rao MVN, Ammermann D (1970) Polytene chromosomes and nucleic acid metabolism during macronuclear development in Euplotes. Chromosoma 29(2):246–254PubMedCrossRefGoogle Scholar
  96. Reed BH, Orr-Weaver TL (1997) The drosophila gene morula inhibits mitotic functions in the endo cell cycle and the mitotic cell cycle. Development 124(18):3543–3553PubMedGoogle Scholar
  97. Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in drosophila. Cell Mol Life Sci 18(12):571–573CrossRefGoogle Scholar
  98. Sarto GE, Stubblefield PA, Therman E (1982) Endomitosis in human trophoblast. Hum Genet 62(3):228–232PubMedCrossRefGoogle Scholar
  99. Scalenghe F et al (1981) Microdissection and cloning of DNA from a specific region of Drosophila Melanogaster polytene chromosomes. Chromosoma 82(2):205–216PubMedCrossRefGoogle Scholar
  100. Schmidt WM et al (2011) DNA damage, somatic aneuploidy, and malignant sarcoma susceptibility in muscular dystrophies. PLoS Genet 7(4):e1002042PubMedPubMedCentralCrossRefGoogle Scholar
  101. Schoenfelder KP, Fox DT (2015) The expanding implications of polyploidy. J Cell Biol 209(4):485–491PubMedPubMedCentralCrossRefGoogle Scholar
  102. Schoenfelder KP et al (2014) Indispensable pre-mitotic endocycles promote aneuploidy in the Drosophila Rectum. Development 141(18):3551–3560PubMedCrossRefGoogle Scholar
  103. Senaratne TN et al (2016) Investigating the interplay between sister chromatid cohesion and homolog pairing in drosophila nuclei. PLoS Genet 12(8):e1006169PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sher N et al (2012) Developmental control of gene copy number by repression of replication initiation and fork progression. Genome Res 22(1):64–75PubMedPubMedCentralCrossRefGoogle Scholar
  105. Sher N et al (2013) Fundamental differences in endoreplication in mammals and drosophila revealed by analysis of endocycling and endomitotic cells. Proc Natl Acad Sci U S A 110(23):9368–9373PubMedPubMedCentralCrossRefGoogle Scholar
  106. Sherman M, Mclaren A, Walker P (1972) Mechanism of accumulation of DNA in giant cells of mouse trophoblast. Nature 238(84):175–176Google Scholar
  107. Skibbens RV (2016) Of rings and rods: regulating Cohesin entrapment of DNA to generate intra- and intermolecular tethers. PLoS Genet 12(10):e1006337PubMedPubMedCentralCrossRefGoogle Scholar
  108. Smith HF et al (2013) Maintenance of interphase chromosome compaction and homolog pairing in drosophila is regulated by the Condensin cap-H2 and its partner Mrg15. Genetics 195(1):127–146PubMedPubMedCentralCrossRefGoogle Scholar
  109. Snow MHL, Ansell JD (1974) The Chromosomes of Giant Trophoblast Cells of the Mouse. Proc R Soc Lond Ser Biol Sci 187(1086):93–98CrossRefGoogle Scholar
  110. Spear BB, Lauth MR (1976) Polytene chromosomes of Oxytricha: biochemical and morphological changes during macronuclear development in a ciliated protozoan. Chromosoma 54(1):1–13PubMedCrossRefGoogle Scholar
  111. Spradling AC, Mahowald AP (1980) Amplification of genes for chorion proteins during oogenesis in Drosophila Melanogaster. Proc Natl Acad Sci 77(2):1096–1100PubMedPubMedCentralCrossRefGoogle Scholar
  112. Stormo BM, Fox DT (2016) Distinct responses to reduplicated chromosomes require distinct Mad2 responses. elife 5Google Scholar
  113. Sumner AT (1998) Induction of diplochromosomes in mammalian cells by inhibitors of topoisomerase II. Chromosoma 107(6–7):486–490PubMedCrossRefGoogle Scholar
  114. Therman E, Denniston C, Sarto GE (1978) Mitotic chiasmata in human diplochromosomes. Hum Genet 45(2):131–135PubMedCrossRefGoogle Scholar
  115. Therman E, Sarto GE, Buchler DA (1983) The structure and origin of giant nuclei in human cancer cells. Cancer Genet Cytogenet 9(1):9–18PubMedCrossRefGoogle Scholar
  116. Tschermak-Woess E, Enzenberg-Kunz U (1965) Die Struktur der Hoch Endopolyploiden Kerne Im Endosperm von Zea Mays, Das Auffallende Verhalten Ihrer Nucleolen und Ihr Endopolyploidiegrad. Planta 64(2):149–169CrossRefGoogle Scholar
  117. Varmuza S et al (1988) Polytene chromosomes in mouse trophoblast giant cells. Development 102(1):127PubMedGoogle Scholar
  118. Vatolina TY et al (2011) Identical functional Organization of Nonpolytene and Polytene Chromosomes in Drosophila Melanogaster. PLoS One 6(10):e25960PubMedPubMedCentralCrossRefGoogle Scholar
  119. Vidwans SJ et al (2002) Sister chromatids fail to separate during an induced Endoreplication cycle in drosophila embryos. Curr Biol 12(10):829–833PubMedPubMedCentralCrossRefGoogle Scholar
  120. Williams BR et al (2007) Disruption of topoisomerase II perturbs pairing in drosophila cell culture. Genetics 177(1):31–46PubMedPubMedCentralCrossRefGoogle Scholar
  121. Wirth KG et al (2006) Separase: a universal trigger for sister chromatid disjunction but not chromosome cycle progression. J Cell Biol 172(6):847–860PubMedPubMedCentralCrossRefGoogle Scholar
  122. Yarosh W, Spradling AC (2014) Incomplete replication generates somatic DNA alterations within drosophila polytene salivary gland cells. Genes Dev 28(16):1840–1855PubMedPubMedCentralCrossRefGoogle Scholar
  123. Yerlici VT, Landweber LF (2014) Programmed genome rearrangements in the ciliate Oxytricha. Microbiol Spectr 2(6). doi: 10.1128/microbiolspec.MDNA3-0025-2014
  124. Zack TI et al (2013) Pan-Cancer patterns of somatic copy number alteration. Nat Genet 45(10):1134–1140PubMedPubMedCentralCrossRefGoogle Scholar
  125. Zhang B et al (2014) Low levels of p53 protein and chromatin silencing of p53 target genes repress apoptosis in drosophila Endocycling cells. PLoS Genet 10(9):e1004581PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zhimulev IF, Belyaeva ES, Semeshin VF, Koryakov DE, Demakov SA, Demakova OV, Pokholkova GV, Andreyeva EN (2004) Polytene Chromosomes: 70 Years of Genetic Research. Int Rev Cytol 241:203-275Google Scholar
  127. Zybina E (1970) Anomalies of polyploidization of the cells of the trophoblast. Tsitologiya 12:1081–1093Google Scholar
  128. Zybina EV, Zybina TG (1996) Polytene Chromosomes in Mammalian Cells. In: Kwang WJ (ed) International Review of Cytology. Academic, Cambridge, pp 53–119Google Scholar
  129. Zybina TG, Stein GI, Zybina EV (2011) Endopolyploid and proliferating trophoblast cells express different patterns of intracellular cytokeratin and glycogen localization in the rat placenta. Cell Biol Int 35(7):649–655PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of Pharmacology and Cancer BiologyDuke University Medical CenterDurhamUSA

Personalised recommendations