Cell to Cell Transfer of the Chromatin-packaged Human Beta-globin Gene Cluster

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2009 Dec 17

PMID 20007595

Citations 18

Authors

Nobutaka Suzuki

Toshihide Itou

Yoshinori Hasegawa

Tsuneko Okazaki

Masashi Ikeno

Affiliations

Soon will be listed here.

Abstract

Cell type-specific gene expression is regulated by chromatin structure and the transcription factors provided by the cells. In the present study, we introduced genes packaged into chromatin into target cells using a human artificial chromosome (HAC) and analyzed regulation of gene expression. The human beta-globin gene cluster was built into an HAC (globin-HAC) and introduced into mouse embryonic stem (ES) cells using microcell-mediated chromosome transfer (MMCT); the adult-type human beta-globin gene was expressed in bone marrow and spleen cells of the transgenic mice. In vitro differentiation of ES cells into mouse erythrocytes indicated that the natural sequential expression of epsilon, gamma and beta-globin genes was reproduced on the globin-HAC. Combination of MMCT and a novel chromosome transfection technique allowed transfer of globin-HAC from HT1080 cells into the human leukemia cell line K562, and from K562 cells back into HT1080 cells. Expression of the gamma-globin gene, repressed in HT1080 cells, was activated in K562 cells without any processes of differentiation into adult erythroid cells, and was completely repressed again in HT1080 cells when transferred back from K562 cells. Thus, transfer of target genes packaged into chromatin using a HAC was useful for functional analyses of gene regulation.

Citing Articles

A cell competition system with one gene expression from a single-copy gene in one cell.

Hasegawa Y, Nakano M, Hosouchi T, Watanabe T, Yamaguchi I, Nakayama M PLoS One. 2024; 19(7):e0302451.

PMID: 38968258 PMC: 11226009. DOI: 10.1371/journal.pone.0302451.

Human Artificial Chromosomes and Their Transfer to Target Cells.

Ponomartsev S, Sinenko S, Tomilin A Acta Naturae. 2022; 14(3):35-45.

PMID: 36348716 PMC: 9611860. DOI: 10.32607/actanaturae.11670.

Pluripotent stem cell-based gene therapy approach: human de novo synthesized chromosomes.

Sinenko S, Ponomartsev S, Tomilin A Cell Mol Life Sci. 2020; 78(4):1207-1220.

PMID: 33011821 PMC: 11072874. DOI: 10.1007/s00018-020-03653-1.

Improving the efficiency of gene insertion in a human artificial chromosome vector and its transfer in human-induced pluripotent stem cells.

Hasegawa Y, Ikeno M, Suzuki N, Nakayama M, Ohara O Biol Methods Protoc. 2020; 3(1):bpy013.

PMID: 32161806 PMC: 6994043. DOI: 10.1093/biomethods/bpy013.

Transfer of Synthetic Human Chromosome into Human Induced Pluripotent Stem Cells for Biomedical Applications.

Sinenko S, Skvortsova E, Liskovykh M, Ponomartsev S, Kuzmin A, Khudiakov A Cells. 2018; 7(12).

PMID: 30544831 PMC: 6316689. DOI: 10.3390/cells7120261.

References

Shen M, Mee P, Nichols J, Yang J, Brook F, Gardner R . A structurally defined mini-chromosome vector for the mouse germ line. Curr Biol. 2000; 10(1):31-4. DOI: 10.1016/s0960-9822(99)00261-4. View

Grosveld F, Van Assendelft G, Greaves D, Kollias G . Position-independent, high-level expression of the human beta-globin gene in transgenic mice. Cell. 1987; 51(6):975-85. DOI: 10.1016/0092-8674(87)90584-8. View

Ikeno M, Masumoto H, Okazaki T . Distribution of CENP-B boxes reflected in CREST centromere antigenic sites on long-range alpha-satellite DNA arrays of human chromosome 21. Hum Mol Genet. 1994; 3(8):1245-57. DOI: 10.1093/hmg/3.8.1245. View

Doherty A, Fisher E . Microcell-mediated chromosome transfer (MMCT): small cells with huge potential. Mamm Genome. 2003; 14(9):583-92. DOI: 10.1007/s00335-003-4002-0. View

Meaburn K, Parris C, Bridger J . The manipulation of chromosomes by mankind: the uses of microcell-mediated chromosome transfer. Chromosoma. 2005; 114(4):263-74. DOI: 10.1007/s00412-005-0014-8. View

Ikeno M, Inagaki H, Nagata K, Morita M, Ichinose H, Okazaki T . Generation of human artificial chromosomes expressing naturally controlled guanosine triphosphate cyclohydrolase I gene. Genes Cells. 2002; 7(10):1021-32. DOI: 10.1046/j.1365-2443.2002.00580.x. View

Suzuki N, Nishii K, Okazaki T, Ikeno M . Human artificial chromosomes constructed using the bottom-up strategy are stably maintained in mitosis and efficiently transmissible to progeny mice. J Biol Chem. 2006; 281(36):26615-23. DOI: 10.1074/jbc.M603053200. View

Ikeno M, Grimes B, Okazaki T, Nakano M, Saitoh K, Hoshino H . Construction of YAC-based mammalian artificial chromosomes. Nat Biotechnol. 1998; 16(5):431-9. DOI: 10.1038/nbt0598-431. View

Kuroiwa Y, Kasinathan P, Choi Y, Naeem R, Tomizuka K, Sullivan E . Cloned transchromosomic calves producing human immunoglobulin. Nat Biotechnol. 2002; 20(9):889-94. DOI: 10.1038/nbt727. View

10.

Basu J, Compitello G, Stromberg G, Willard H, Van Bokkelen G . Efficient assembly of de novo human artificial chromosomes from large genomic loci. BMC Biotechnol. 2005; 5:21. PMC: 1182356. DOI: 10.1186/1472-6750-5-21. View

11.

Kuroiwa Y, Tomizuka K, Shinohara T, Kazuki Y, Yoshida H, Ohguma A . Manipulation of human minichromosomes to carry greater than megabase-sized chromosome inserts. Nat Biotechnol. 2000; 18(10):1086-90. DOI: 10.1038/80287. View

12.

de Jong G, Telenius A, Vanderbyl S, Meitz A, Drayer J . Efficient in-vitro transfer of a 60-Mb mammalian artificial chromosome into murine and hamster cells using cationic lipids and dendrimers. Chromosome Res. 2001; 9(6):475-85. DOI: 10.1023/a:1011680529073. View

13.

Gaensler K, Kitamura M, Kan Y . Germ-line transmission and developmental regulation of a 150-kb yeast artificial chromosome containing the human beta-globin locus in transgenic mice. Proc Natl Acad Sci U S A. 1993; 90(23):11381-5. PMC: 47986. DOI: 10.1073/pnas.90.23.11381. View

14.

Larin Z, Mejia J . Advances in human artificial chromosome technology. Trends Genet. 2002; 18(6):313-9. DOI: 10.1016/S0168-9525(02)02679-3. View

15.

Peterson K, Zitnik G, Huxley C, Lowrey C, Gnirke A, Leppig K . Use of yeast artificial chromosomes (YACs) for studying control of gene expression: correct regulation of the genes of a human beta-globin locus YAC following transfer to mouse erythroleukemia cell lines. Proc Natl Acad Sci U S A. 1993; 90(23):11207-11. PMC: 47951. DOI: 10.1073/pnas.90.23.11207. View

16.

Kazuki Y, Shinohara T, Tomizuka K, Katoh M, Ohguma A, Ishida I . Germline transmission of a transferred human chromosome 21 fragment in transchromosomal mice. J Hum Genet. 2001; 46(10):600-3. DOI: 10.1007/s100380170028. View

17.

Li Q, Peterson K, Fang X, Stamatoyannopoulos G . Locus control regions. Blood. 2002; 100(9):3077-86. PMC: 2811695. DOI: 10.1182/blood-2002-04-1104. View

18.

Suwabe N, Takahashi S, Nakano T, Yamamoto M . GATA-1 regulates growth and differentiation of definitive erythroid lineage cells during in vitro ES cell differentiation. Blood. 1998; 92(11):4108-18. View

19.

Peterson K, Clegg C, Huxley C, JOSEPHSON B, Haugen H, Furukawa T . Transgenic mice containing a 248-kb yeast artificial chromosome carrying the human beta-globin locus display proper developmental control of human globin genes. Proc Natl Acad Sci U S A. 1993; 90(16):7593-7. PMC: 47188. DOI: 10.1073/pnas.90.16.7593. View

20.

Ebersole T, Ross A, Clark E, McGill N, Schindelhauer D, Cooke H . Mammalian artificial chromosome formation from circular alphoid input DNA does not require telomere repeats. Hum Mol Genet. 2000; 9(11):1623-31. DOI: 10.1093/hmg/9.11.1623. View