Preview

Вавиловский журнал генетики и селекции

Расширенный поиск

Пространственно-временная организация репликации у дрозофилы и ее особенности в политенных хромосомах

https://doi.org/10.18699/VJ19.473

Аннотация

Drosophila melanogaster – один из популярных модельных организмов для изучения репликации ДНК. Начиная с 1960-х годов репликацию политенных хромосом активно изучали c помощью цитологических методов. В последние двадцать лет прогресс в изучении репликации определялся применением новых методов. Использование флуоресцентных красителей значительно улучшило разрешение цитологических подходов. Наличие геномной последовательности позволило изучить и соотнести репликацию ДНК со структурой хроматина и активностью генов для эухроматиновых районов в масштабе генома. Картирование границ цитологических структур политенных хромосом на последовательности генома дало возможность сравнить временные характеристики репликации районов хромосом в клеточных культурах и клетках слюнной железы. Были описаны новые особенности репликации как для хромосом диплоидных клеток, так и для политенных хромосом дрозофилы. Анализ временных профилей репликации показал, что организация репликации имеет в своей основе те же закономерности, что и у других хорошо изученных с точки зрения репликации видов, в частности человека. Ранняя репликация, как правило, приурочена к районам, характеризующимся высоким уровнем транскрипции, высокой плотностью генов и присутствием множественных сайтов потенциальной инициации репликации. Компактность генома D. melanogaster вносит некоторые особенности в организацию ее репликации. Последовательность репликации генома в политенных хромосомах и хромосомах диплоидных клеток имеет много общего: инициация репликации приурочена к одним и тем же районам, между которыми лежат протяженные участки генома, где репликация происходит преимущественно от краев к середине. Важнейшими особенностями репликации в политенных хромосомах являются низкая скорость репликационных вилок и зависимость протяженности S-фазы от множества как внутренних, так и внешних факторов. В политенных хромосомах D. melanogaster скорость движения репликационных вилок зависит от присутствия в хроматине белков SUUR и Rif1.

Об авторах

Т. Д. Колесникова
Институт молекулярной и клеточной биологии Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университет.
Россия
Новосибирск.


О. В. Антоненко
Институт молекулярной и клеточной биологии Сибирского отделения Российской академии наук.
Россия
Новосибирск.


И. В. Макунин
Институт молекулярной и клеточной биологии Сибирского отделения Российской академии наук; Исследовательский вычислительный центр, Квинслендский университет.
Россия
Новосибирск; Сент-Люсия, Квинсленд, Австралия.


Список литературы

1. Achary P.M., Majumdar K., Duttagupta A., Mukherjee A.S. Replication of DNA in larval salivary glands of Drosophila after in vivo synchro¬nization. Chromosoma. 1981;82(4):505-514.

2. Allison L., Arndt-Jovin D.J., Gratzner H., Ternynck T., Robert-Ni- coud M. Mapping of the pattern of DNA replication in polytene chromosome from Chironomus thummi using monoclonal anti-bro- modeoxyuridine antibodies. Cytometry. 1985;6(6):584-590.

3. Amabis J.M. Induction of DNA synthesis in Rhynchosciara angelae salivary gland. Cell Differ. 1974;3(4):199-207.

4. Andreyeva E.N., Bernardo T.J., Kolesnikova T.D., Lu X., Yari- nich L.A., Bartholdy B.A., Guo X., Posukh O.V., Healton S., Will- cockson M.A., Pindyurin A.V., Zhimulev I.F., Skoultchi A.I., Fyo¬dorov D.V Regulatory functions and chromatin loading dynamics of linker histone H1 during endoreplication in Drosophila. Genes Dev. 2017;31(6):603-616.

5. Bedo D.G. Patterns of polytene-chromosome replication in Simulium ornatipes (Diptera: Simuliidae). Genetica. 1982;59:9-21.

6. Belyakin S.N., Babenko V.N., Maksimov D.A., Shloma V.V., Kvon E.Z., Belyaeva E.S., Zhimulev I.F. Gene density profile re¬veals the marking of late replicated domains in the Drosophila mela- nogaster genome. Chromosoma. 2010;119(6):589-600.

7. Berezney R., Dubey D.D., Huberman J.A. Heterogeneity of eukaryo¬tic replicons, replicon clusters, and replication foci. Chromosoma. 2000;108:471-484.

8. Borowiec J.A., Schildkraut C.L. Open sesame: activating dormant rep-lication origins in the mouse immunoglobulin heavy chain (Igh) lo¬cus. Curr. Opin. Cell Biol. 2011;23:284-292.

9. Boulos R.E., Drillon G., Argoul F., Arneodo A., Audit B. Structural or¬ganization of human replication timing domains. FEBS Lett. 2015; 589(20 Pt A):2944-2957.

10. Britton J.S., Edgar B.A. Environmental control of the cell cycle in Dro¬sophila: nutrition activates mitotic and endoreplicative cells by dis¬tinct mechanisms. Development. 1998;125:2149-2158.

11. Britton J.S., Lockwood W.K., Li L., Cohen S.M., Edgar B.A. Droso-phila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell. 2002;2:239-249.

12. Cadoret J.C., Meisch F., Hassan-Zadeh V, Luyten I., Guillet C., Du- ret L., Quesneville H., Prioleau M.N. Genome-wide studies high-light indirect links between human replication origins and gene regulation. Proc. Natl. Acad. Sci. USA. 2008;105(41):15837-15842.

13. Cayrou C., Coulombe P., Vigneron A., Stanojcic S., Ganier O., Peif- fer I., Rivals E., Puy A., Laurent-Chabalier S., Desprat R., Mecha- li M. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 2011;21:1438-1449.

14. Chagin V.O., Stear J.H., Cardoso M.C. Organization of DNA replica-tion. Cold Spring Harb. Perspect. Biol. 2010;2:a000737.

15. Cordeiro M., Meneghini R. The rate of DNA replication in the polytene chromosomes of Rhynchosciara angelae. J. Mol. Biol. 1973;78(2): 261-274.

16. Danieli G.A., Rodino E. Larval moulting cycle and DNA synthesis in Drosophila hydei salivary glands. Nature. 1967; 213(5074):424- 425.

17. Debatisse M., Le Tallec B., Letessier A., Dutrillaux B., Brison O. Com¬mon fragile sites: mechanisms of instability revisited. Trends Genet. 2012;28(1):22-32.

18. Demontis F., Perrimon N. Integration of Insulin receptor/Foxo signal-ing and dMyc activity during muscle growth regulates body size in Drosophila. Development. 2009;136:983-993.

19. Doronkin S., Djagaeva I., Beckendorf S.K. The COP9 signalosome promotes degradation of Cyclin E during early Drosophila oogene-sis. Dev. Cell. 2003;4(5):699-710.

20. Durkin S.G., Glover T.W. Chromosome fragile sites. Annu. Rev. Genet. 2007;41:169-192.

21. Duronio R.J., O’Farrell P.H. Developmental control of the G1 to S tran¬sition in Drosophila: cyclin E is a limiting downstream target of E2F. Genes Dev. 1995;9(12):1456-1468.

22. Edgar B.A., Orr-Weaver T.L. Endoreplication cell cycles: more for less. Cell. 2001;105(3):297-306.

23. Edgar B.A., Zielke N., Gutierrez C. Endocycles: a recurrent evolution-ary innovation for post-mitotic cell growth. Nat. Rev. Mol. Cell Biol. 2014;15(3):197-210.

24. Gibert J.M., Karch F. The Polycomb group protein CRAMPED is in-volved with TRF2 in the activation of the histone H1 gene. Chromo¬soma. 2011;120:297-307.

25. Gilbert D.M. Replication timing and transcriptional control: beyond cause and effect. Curr. Opin. Cell Biol. 2002;14(3):377-383.

26. Gilbert D.M., Cohen S.N. Bovine papilloma virus plasmids replicate randomly in mouse fibroblasts throughout S phase of the cell cycle. Cell. 1987;50(1):59-68.

27. Gilbert D.M., Takebayashi S.I., Ryba T., Lu J., Pope B.D., Wilson K.A., Hiratani I. Space and time in the nucleus: developmental control of replication timing and chromosome architecture. Cold Spring Harb. Symp. Quant. Biol. 2010;75:143-153.

28. Gillespie P.J., Blow J.J. Clusters, factories and domains: the complex structure of S-phase comes into focus. Cell Cycle. 2010;9:3218- 3226.

29. Grewal S.S., Li L., Orian A., Eisenman R.N., Edgar B.A. Myc-depen- dent regulation of ribosomal RNA synthesis during Drosophila de-velopment. Nat. Cell Biol. 2005;7(3):295-302.

30. Guilbaud G., Rappailles A., Baker A., Chen C.L., Arneodo A., Gol- dar A., d’Aubenton-Carafa Y., Thermes C., Audit B., Hyrien O. Evidence for sequential and increasing activation of replication ori¬gins along replication timing gradients in the human genome. PLoS Comput. Biol. 2011;7(12):e1002322.

31. Hassel C., Zhang B., Dixon M., Calvi B.R. Induction of endocycles represses apoptosis independently of differentiation and predisposes cells to genome instability. Development. 2014;141(1):112-123.

32. Hagele K. Prolongation of replication time after doubling of the DNA content of polytene chromosome bands of Chironomus. Chromo-soma. 1976;55(3):253-258.

33. Hiratani I., Gilbert D.M. Replication timing as an epigenetic mark. Epi- genetics. 2009;4(2):93-97.

34. Hiratani I., Ryba T., Itoh M., Rathjen J., Kulik M., Papp B., Fussner E., Bazett-Jones D.P., Plath K., Dalton S., Rathjen P.D., Gilbert D.M. Genome-wide dynamics of replication timing revealed by in vitro models of mouse embryogenesis. Genome Res. 2010;20:155-169.

35. Hiratani I., Ryba T., Itoh M., Yokochi T., Schwaiger M., Chang C.W., Lyou Y., Townes T.M., Schubeler D., Gilbert D.M. Global reorgani¬zation of replication domains during embryonic stem cell differen¬tiation. PLoS Biol. 2008;6:e245.

36. Hong A., Narbonne-Reveau K., Riesgo-Escovar J., Fu H., Ala- djem M.I., Lilly M.A. The cyclin-dependent kinase inhibitor Da- capo promotes replication licensing during Drosophila endocycles. EMBO. J. 2007;26(8):2071-2082.

37. Hua B.L., Bell G.W., Kashevsky H., Von Stetina J.R., Orr-Weaver T.L. Dynamic changes in ORC localization and replication fork progres¬sion during tissue differentiation. BMC Genomics. 2018;19(1):623.

38. Jackson D.A., Pombo A. Replicon clusters are stable units of chromo-some structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 1998;140(6):1285-1295.

39. Jackson L.P., Reed S.I., Haase S.B. Distinct mechanisms control the stability of the related S-phase cyclins Clb5 and Clb6. Mol. Cell. Biol. 2006;26:2456-2466.

40. Julienne H., Zoufir A., Audit B., Arneodo A. Human genome replica-tion proceeds through four chromatin states. PLoS Comput. Biol. 2013;9(10):e1003233.

41. Keyl H.-G. Duplikationen von untereinheiten der chromosomalen DNS wahrend der Evolution von Chironomus thummi. Chromosoma. 1965;17:139-180.

42. Keyl H.-G., Pelling C. Differentielle DNS-Replikation in den Spei- cheldrusen-chromosopmen von Chironomus thummi. Chromosoma. 1963;14:347-359.

43. Kolesnikova T.D., Goncharov F.P., Zhimulev I.F. Similarity in replica¬tion timing between polytene and diploid cells is associated with the organization of the Drosophila genome. PLoS One. 2018;13(4): e0195207.

44. Kolesnikova T.D., Makunin I.V., Volkova E.I., Pirrotta V, Belya¬eva E.S., Zhimulev I.F. Functional dissection of the Suppressor of UnderReplication protein of Drosophila melanogaster: identifica-tion of domains influencing chromosome binding and DNA replication. Genetica. 2005;124:187-200.

45. Kolesnikova T.D., Posukh O.V., Andreyeva E.N., Bebyakina D.S., Ivankin A.V., Zhimulev I.F. Drosophila SUUR protein associates with PCNA and binds chromatin in a cell cycle-dependent manner. Chromosoma. 2013;122(1-2):55-66.

46. Kolesnikova T.D., Semeshin V.F., Andreyeva E.N., Zykov I.A., Koko- za E.B., Kalashnikova D.A., Belyaeva E.S., Zhimulev I.F. Induced decondensation of heterochromatin in Drosophila melanogaster polytene chromosomes under condition of ectopic expression of the Supressor of underreplication gene. Fly(Austin). 2011;5(3):181- 190.

47. Koryakov D.E., Walther M., Ebert A., Lein S., Zhimulev I.F., Reuter G. The SUUR protein is involved in binding of SU(VAR)3-9 and me- thylation of H3K9 and H3K27 in chromosomes of Drosophila mela- nogaster. Chromosome Res. 2011;19(2):235-249.

48. Koryakov D.E., Zhimulev I.F. DNA replication in nurse cell polytene chromosomes of Drosophila melanogaster otu mutants. Chromo-soma. 2015;124:95-106.

49. Kozlova T., Semeshin V.F., Tretyakova I.V., Kokoza E.B., Pirrotta V, Grafodatskaya V.E., Belyaeva E.S., Zhimulev I.F. Molecular and cytogenetical characterization of the 10A1-2 band and adjoining re¬gion in the Drosophila melanogaster polytene X chromosome. Ge¬netics. 1994;136:1063-1073.

50. Lakhotia S.C., Sinha P. Replication in Drosophila chromosomes. X. Two kinds of active replicons in salivary gland polytene nuclei and their relation to chromosomal replication patterns. Chromosoma. 1983;88(4):265-276.

51. Lebofsky R., Heilig R., Sonnleitner M., Weissenbach J., Bensimon A. DNA replication origin interference increases the spacing between initiation events in human cells. Mol. Biol. Cell. 2006;17:5337- 5345.

52. Lee H.O., Davidson J.M., Duronio R.J. Endoreplication: polyploidy with purpose. Genes Dev. 2009;23:2461-2477.

53. Lilly M.A., Duronio R.J. New insights into cell cycle control from the Drosophila endocycle. Oncogene. 2005;24(17):2765-2775.

54. Lilly M.A., Spradling A.C. The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev. 1996;10:2514-2526.

55. Lubelsky Y., Prinz J.A., DeNapoli L., Li Y., Belsky J.A., MacAl- pine D.M. DNA replication and transcription programs respond to the same chromatin cues. Genome Res. 2014;24:1102-1114.

56. Ma H., Samarabandu J., Devdhar R.S., Acharya R., Cheng P.C., Meng C., Berezney R. Spatial and temporal dynamics of DNA re¬plication sites in mammalian cells. J. Cell Biol. 1998; 143:1415¬1425.

57. MacAlpine H.K., Gordan R., Powell S.K., Hartemink A.J., MacAl- pine D.M. Drosophila ORC localizes to open chromatin and marks sites of cohesin complex loading. Genome Res. 2010;20:201-211.

58. MacAlpine D.M., Rodriguez H.K., Bell S.P. Coordination of replica-tion and transcription along a Drosophila chromosome. Genes Dev. 2004;18(24):3094-3105.

59. Maqbool S.B., Mehrotra S., Kolpakas A., Durden C., Zhang B., Zhong H., Calvi B.R. Dampened activity of E2F1-DP and Myb- MuvB transcription factors in Drosophila endocycling cells. J. Cell Sci. 2010;123(Pt 23):4095-4106.

60. Meneghini R., Cordeiro M. DNA replication in polytene chromosomes of Rhynchosciara angelae. Cell Differ. 1972;1(3):167-177.

61. Mesner L.D., Valsakumar V, Karnani N., Dutta A., Hamlin J.L., Beki- ranov S. Bubble-chip analysis of human origin distributions demon¬strates on a genomic scale significant clustering into zones and significant association with transcription. Genome Res. 2011;21: 377-389.

62. Moberg K.H., Bell D.W., Wahrer D.C., Haber D.A., Hariharan I.K. Ar-chipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature. 2001;413(6853):311-316.

63. Mulder M.P., van Duijn P., Gloor H.J. The replicative organization of DNA in polytene chromosomes of Drosophila hydei. Genetica. 1968;39(3):385-428.

64. Munden A., Rong Z., Sun A., Gangula R., Mallal S., Nordman J.T. Rif1 inhibits replication fork progression and controls DNA copy number in Drosophila. Elife. 2018;7:e39140.

65. Nordman J.T., Kozhevnikova E.N., Verrijzer C.P., Pindyurin A.V., Andreyeva E.N., Shloma V.V., Zhimulev I.F., Orr-Weaver T.L. DNA copy-number control through inhibition of replication fork progres¬sion. Cell Rep. 2014;9(3):841-849.

66. Norio P., Kosiyatrakul S., Yang Q., Guan Z., Brown N.M., Thomas S., Riblet R., Schildkraut C.L. Progressive activation of DNA replica¬tion initiation in large domains of the immunoglobulin heavy chain locus during B cell development. Mol. Cell. 2005;20:575-587.

67. Peric-Hupkes D., Meuleman W., Pagie L., Bruggeman S.W., Solovei I., Brugman W., Graf S., Flicek P., Kerkhoven R.M., van Lohuizen M., Reinders M., Wessels L., van Steensel B. Molecular maps of the reorganization of genome-nuclear lamina interactions during differ¬entiation. Mol. Cell. 2010;38(4):603-613.

68. Petrov D.A. DNA loss and evolution of genome size in Drosophila. Genetica. 2002;115(1):81-91.

69. Petryk N., Kahli M., d’Aubenton-Carafa Y., Jaszczyszyn Y., Shen Y., Silvain M., Thermes C., Chen C.L., Hyrien O. Replication landscape of the human genome. Nat. Commun. 2016;7:10208.

70. Pickersgill H., Kalverda B., de Wit E., Talhout W., Fornerod M., van Steensel B. Characterization of the Drosophila melanogaster ge-nome at the nuclear lamina. Nat. Genet. 2006;38(9):1005-1014.

71. Pierce S.B., Yost C., Britton J.S., Loo L.W., Flynn E.M., Edgar B.A., Eisenman R.N. dMyc is required for larval growth and endorepli-cation in Drosophila. Development. 2004;131(10):2317-2327.

72. Plaut W., Nash D., Fanning T. Ordered replication of DNA in poly- tene chromosomes of Drosophila melanogaster. J. Mol. Biol. 1966; 16:85-93.

73. Pokholkova G.V., Koryakov D.E., Pindyurin A.V., Kozhevnikova E.N., Belyakin S.N., Andreyenkov O.V., Belyaeva E.S., Zhimulev I.F. Tethering of SUUR and HP1 proteins results in delayed replication of euchromatic regions in Drosophila melanogaster polytene chro¬mosomes. Chromosoma. 2015;124(2):209-220.

74. Pope B.D., Hiratani I., Gilbert D.M. Domain-wide regulation of DNA replication timing during mammalian development. Chromosome Res. 2010;18(1):127-136.

75. Pope B.D., Ryba T., Dileep V, Yue F., Wu W., Denas O., Vera D.L., Wang Y., Hansen R.S., Canfield T.K., Thurman R.E., Cheng Y., Gulsoy G., Dennis J.H., Snyder M.P., Stamatoyannopoulos J.A., Taylor J., Hardison R.C., Kahveci T., Ren B., Gilbert D.M. Topo-logically associating domains are stable units of replication-timing regulation. Nature. 2014;515(7527):402-405.

76. Posukh O.V., Maksimov D.A., Laktionov P.P., Koryakov D.E., Belya¬kin S.N. Functional dissection of Drosophila melanogaster SUUR protein influence on H3K27me3 profile. Epigenetics Chromatin. 2017;10(1):56.

77. Posukh O.V., Maksimov D.A., Skvortsova K.N., Koryakov D.E., Be-lyakin S.N. The effects of SUUR protein suggest its role in repres-sive chromatin renewal during replication in Drosophila. Nucleus. 2015;6(4):249-253.

78. Prioleau M.N., MacAlpine D.M. DNA replication origins-where do we begin? Genes Dev. 2016;30:1683-1697.

79. Redfern C.P.F. DNA replication in polytene chromosomes: Similarity of termination patterns in somatic and germ-line derived polytene chromosomes of Anopheles stephensi liston (Diptera: Culicidae). Chromosoma. 1981;84:33-47.

80. Rhind N., Gilbert D.M. DNA replication timing. Cold Spring Harb. Perspect. Biol. 2013;5(8):a010132.

81. Royzman I., Orr-Weaver T.L. S phase and differential DNA replication during Drosophila oogenesis. Genes Cells. 1998;3:767-776.

82. Rudkin G.T. Replication in polytene chromosomes. Ed. W. Beermann. Results and Problems in Cell Differentiation. Berlin; Heidelberg; New York: Springer-Verlag, 1972;4:59-85.

83. Rudkin G.T. Cyclic synthesis of DNA in polytene chromosomes of Diptera. Eds. M. Balls, F. Billet. Cell Cycle in Development and Differentiation. London: Cambridge Univ. Press, 1973;279-292.

84. Saucedo L.J., Gao X., Chiarelli D.A., Li L., Pan D., Edgar B.A. Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat. Cell Biol. 2003;5(6):566-571.

85. Schubeler D., Scalzo D., Kooperberg C., van Steensel B., Delrow J., Groudine M. Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat. Genet. 2002;32(3):438-442.

86. Schwaiger M., Stadler M.B., Bell O., Kohler H., Oakeley E.J., Schube- ler D. Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev. 2009;23:589-601.

87. Seller C.A., O’Farrell P.H. Rif1 prolongs the embryonic S phase at the Drosophila mid-blastula transition. PLoS Biol. 2018; 16(5): e2005687.

88. Shcherbata H.R., Althauser C., Findley S.D., Ruohola-Baker H. The mitotic-to-endocycle switch in Drosophila follicle cells is executed by Notch-dependent regulation of G1/S, G2/M and M/G1 cell-cycle transitions. Development. 2004;131(13):3169-3181.

89. Sher N., Bell G.W., Li S., Nordman J., Eng T., Eaton M.L., Macal- pine D.M., Orr-Weaver T.L. Developmental control of gene copy number by repression of replication initiation and fork progression. Genome Res. 2012;22(1):64-75.

90. Sher N., von Stetina J.R., Bell G.W., Matsuura S., Ravid K., Orr-We- aver T.L. Fundamental differences in endoreplication in mammals and Drosophila revealed by analysis of endocycling and endomitotic cells. Proc. Natl. Acad. Sci. USA. 2013;110(23):9368-9373.

91. Shirahige K., Hori Y., Shiraishi K., Yamashita M., Takahashi K., Obu- se C., Tsurimoto T., Yoshikawa H. Regulation of DNA-replication origins during cell-cycle progression. Nature. 1998;395(6702): 618-621.

92. Shu Z., Row S., Deng W.M. Endoreplication: The Good, the Bad, and the Ugly. Trends Cell. Biol. 2018;28(6):465-474.

93. Sinha P., Mishra A., Lakhotia S.C. Chromosomal organization of Dro-sophila tumours. I. Polytene chromosome organization and DNA synthesis in ovarian pseudonurse cells in otu mutants of D. melano- gaster. Chromosoma. 1987;95:108-116.

94. Smith A.V., Orr-Weaver T.L. The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development. 1991;112:997-1008.

95. Spierer A., Spierer P. Similar level of polyteny in bands and interbands of Drosophila giant chromosomes. Nature. 1984;307:176-178.

96. Sreesankar E., Bharathi V, Mishra R.K., Mishra K. Drosophila Rifl is an essential gene and controls late developmental events by direct interaction with PP1-87B. Sci. Rep. 2015;5:10679.

97. Steinemann M. Chromosomal replication of Drosophila virilis. II. Or-ganization of active origins in diploid brain cells. Chromosoma. 1981a;82(2):267-288.

98. Steinemann M. Chromosomal replication in Drosophila virilis. III. Or-ganization of active origins in the highly polytene salivary gland cells. Chromosoma. 1981b;82(2):289-307.

99. Stocker A.J., Pavan C. The influence of ecdysterone on gene ampli-fication, DNA synthesis, and puff formation in the salivary gland chromosomes of Rhynchosciara hollaenderi. Chromosoma. 1974; 45(3):295-319.

100. Su T.T., O’Farrell P.H. Chromosome association of minichromosome maintenance proteins in Drosophila endoreplication cycles. J. Cell. Biol. 1998;140(3):451-460.

101. Sun J., Smith L., Armento A., Deng W.M. Regulation of the endocycle/ gene amplification switch by Notch and ecdysone signaling. J. Cell Biol. 2008;182(5):885-896.

102. Swanson C.I., Meserve J.H., McCarter P.C., Thieme A., Mathew T., Elston T.C., Duronio R.J. Expression of an S phase-stabilized ver-sion of the CDK inhibitor Dacapo can alter endoreplication. Deve-lopment. 2015;142(24):4288-4298.

103. Taniue K., Nishida A., Hamada F., Sugie A., Oda T., Ui-Tei K., Ta- bata T., Akiyama T. Sunspot, a link between Wingless signaling and endoreplication in Drosophila. Development. 2010;137(10):1755- 1764.

104. Vatolina T.Y., Boldyreva L.V., Demakova O.V., Demakov S.A., Ko- koza E.B., Semeshin V.F., Babenko V.N., Goncharov F.P., Belya-eva E.S., Zhimulev I.F. Identical functional organization of nonpoly- tene and polytene chromosomes in Drosophila melanogaster. PLoS One. 2011;6:e25960.

105. Volkova E.I., Yurlova A.A., Kolesnikova T.D., Makunin I.V., Zhimu¬lev I.F. Ectopic expression of the Suppressor of Underreplication gene inhibits endocycles but not the mitotic cell cycle in Drosophila melanogaster. Mol. Genet. Genomics. 2003;270:387-393. White E.J., Emanuelsson O., Scalzo D., Royce T., Kosak S., Oake- ley E.J., Weissman S., Gerstein M., Groudine M., Snyder M., Schu- beler D. DNA replication-timing analysis of human chromosome 22 at high resolution and different developmental states. Proc. Natl. Acad. Sci. USA. 2004;101(51):17771-17776.

106. Willis N., Rhind N. Regulation of DNA replication by the S-phase DNA damage checkpoint. Cell Div. 2009;4:13.

107. Woodfine K., Beare D.M., Ichimura K., Debernardi S., Mungall A.J., Fiegler H., Collins V.P., Carter N.P., Dunham I. Replication timing of human chromosome 6. Cell Cycle. 2005;4:172-176.

108. Zhimulev I.F. Genetic organization of polytene chromosomes. Adv. Genet. 1999;39:1-589.

109. Zhimulev I.F., Belyaeva E.S., Makunin I.V., Pirrotta V., Volkova E.I., Alekseyenko A.A., Andreyeva E.N., Makarevich G.F., Boldyre¬va L.V., Nanayev R.A., Demakova O.V. Influence of the SuUR gene on intercalary heterochromatin in Drosophila melanogaster poly- tene chromosomes. Chromosoma. 2003;111:377-398.

110. Zhimulev I.F., Zykova T.Y., Goncharov F.P., Khoroshko V.A., Dema¬kova O.V., Semeshin V.F., Pokholkova G.V., Boldyreva L.V., Demi¬dova D.S., Babenko V.N., Demakov S.A., Belyaeva E.S. Genetic organization of interphase chromosome bands and interbands in Drosophila melanogaster. PLoS One. 2014;9:e101631.

111. Zielke N., Edgar B.A., DePamphilis M.L. Endoreplication. Cold Spring Harb. Perspect. Biol. 2013;5(1):a012948.

112. Zielke N., Kim K.J., Tran V., Shibutani S.T., Bravo M.J., Nagara- jan S., van Straaten M., Woods B., von Dassow G., Rottig C., Leh- ner C.F., Grewal S.S., Duronio R.J., Edgar B.A. Control of Drosophla endocycles by E2F and CRL4(CDT2). Nature. 2011;480(7375): 123-127.


Рецензия

Просмотров: 1093


Creative Commons License
Контент доступен под лицензией Creative Commons Attribution 4.0 License.


ISSN 2500-3259 (Online)