The β-interferon scaffold attachment region confers high-level transgene expression and avoids extinction by epigenetic modifications of integrated provirus in adipose tissue-derived human mesenchymal stem cells

Tissue Engineering - Part C: Methods

Volumn 17, Issue 3, 2011, Pages 275-287

  Moreno, Rafael ^a   Martínez, Itziar ^a   Petriz, Jordi ^b   Nadal, Marga ^c   Tintoré, Xavier ^d   Gonzalez, Juan Ramón ^e   Gratacós, Eduard ^f   Aran, Josep M ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^d HOSPITAL GENERAL DE CATALUNYA   (Spain)

^e CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^f INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; ANTIBIOTICS; GENE THERAPY; GENETIC ENGINEERING; GLYCOPROTEINS; PROTEINS; SCAFFOLDS; STEM CELLS; TISSUE; VECTORS;

ADIPOCYTES; ADIPOSE TISSUE; ADIPOSE TISSUE-DERIVED MESENCHYMAL STEM CELLS; BOUNDARY ELEMENTS; DEACETYLATION; DIFFERENTIATION PROCESS; DINUCLEOTIDES; EPIGENETIC MODIFICATION; HISTONE ACETYLATION; HUMAN MESENCHYMAL STEM CELLS; LONG TERM DYNAMICS; LONG TERMINAL REPEATS; OSTEOCYTES; PARACRINE; REPAIR STRATEGY; RETROVIRAL VECTORS; TRANSGENE; TRANSGENE EXPRESSION;

CELL CULTURE;

BETA INTERFERON; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HISTONE;

ACETYLATION; ADIPOCYTE; ADIPOSE TISSUE; ADULT; ANIMAL; ARTICLE; CELL DIFFERENTIATION; CHICKEN; CYTOLOGY; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE VECTOR; GENETIC EPIGENESIS; GENETIC TRANSDUCTION; GENETICS; HUMAN; INSULATOR ELEMENT; MATRIX ATTACHMENT REGION; MESENCHYMAL STEM CELL; METABOLISM; OSTEOCYTE; PROVIRUS; RETROVIRUS; TIME; TRANSGENE; VIROLOGY; VIRUS DNA CELL DNA INTERACTION;

ACETYLATION; ADIPOCYTES; ADIPOSE TISSUE; ADULT; ANIMALS; CELL DIFFERENTIATION; CHICKENS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HISTONES; HUMANS; INSULATOR ELEMENTS; INTERFERON-BETA; MATRIX ATTACHMENT REGIONS; MESENCHYMAL STEM CELLS; OSTEOCYTES; PROVIRUSES; RETROVIRIDAE; TIME FACTORS; TRANSDUCTION, GENETIC; TRANSGENES; VIRUS INTEGRATION;

EID: 79952165229     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2010.0383     Document Type: Article

References (49)

1. Bunnell, B. A., Flaat, M., Gagliardi, C., Patel, B., and Ripoll, C. Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45, 115, 2008.
2. Zuk, P. A., Zhu, M., Ashjian, P., De Ugarte, D. A., Huang, J. I., Mizuno, H., et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13, 4279, 2002.
3. Schaffler, A., and Buchler, C. Concise review: adipose tissuederived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 25, 818, 2007.
4. Phinney, D. G., and Prockop, D. J. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25, 2896, 2007.
5. Puissant, B., Barreau, C., Bourin, P., Clavel, C., Corre, J., Bousquet, C., et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 129, 118, 2005.
6. Rasmusson, I. Immune modulation by mesenchymal stem cells. Exp Cell Res 312, 2169, 2006.
7. Yanez, R., Lamana, M. L., Garcia-Castro, J., Colmenero, I., Ramirez, M., and Bueren, J. A. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24, 2582, 2006.
8. Izadpanah, R., and Bunnell, B. A. Gene delivery to mesenchymal stem cells. Methods Mol Biol 449, 153, 2008.
9. Eliopoulos, N., Francois, M., Boivin, M. N., Martineau, D., and Galipeau, J. Neo-organoid of marrow mesenchymal stromal cells secreting interleukin-12 for breast cancer therapy. Cancer Res 68, 4810, 2008.
10. Kucerova, L., Altanerova, V., Matuskova, M., Tyciakova, S., and Altaner, C. Adipose tissue-derived human mesenchymal stem cells mediated prodrug cancer gene therapy. Cancer Res 67, 6304, 2007.
11. Compte, M., Cuesta, A. M., Sanchez-Martin, D., Alonso-Camino, V., Vicario, J. L., Sanz, L., et al. Tumor immunotherapy using gene-modified human mesenchymal stem cells loaded into synthetic extracellular matrix scaffolds. Stem Cells 27, 753, 2009.
12. Ellis, J. Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum Gene Ther 16, 1241, 2005.
13. Agarwal, M., Austin, T. W., Morel, F., Chen, J., Bohnlein, E., and Plavec, I. Scaffold attachment region-mediated enhancement of retroviral vector expression in primary T cells. J Virol 72, 3720, 1998.
14. Dang, Q., Auten, J., and Plavec, I. Human beta interferon scaffold attachment region inhibits de novo methylation and confers long-term, copy number-dependent expression to a retroviral vector. J Virol 74, 2671, 2000.
15. Emery, D. W., Yannaki, E., Tubb, J., and Stamatoyannopoulos, G. A chromatin insulator protects retrovirus vectors from chromosomal position effects. Proc Natl Acad Sci U S A 97, 9150, 2000.
16. Li, C. L., and Emery, D. W. The cHS4 chromatin insulator reduces gammaretroviral vector silencing by epigenetic modifications of integrated provirus. Gene Ther 15, 49, 2008.
17. Rivella, S., Callegari, J. A., May, C., Tan, C. W., and Sadelain, M. The cHS4 insulator increases the probability of retroviral expression at random chromosomal integration sites. J Virol 74, 4679, 2000.
18. Hildinger, M., Abel, K. L., Ostertag, W., and Baum, C. Design of 50 untranslated sequences in retroviral vectors developed for medical use. J Virol 73, 4083, 1999.
19. Moreno, R., Martinez, I., Petriz, J., Gonzalez, J. R., Gratacos, E., and Aran, J. M. Boundary sequences stabilize transgene expression from subtle position effects in retroviral vectors. Blood Cells Mol Dis 43, 214, 2009.
20. Rice, P., Longden, I., and Bleasby, A. EMBOSS: the European molecular biology open software suite. Trends Genet 16, 276, 2000.
21. Aranyi, T., Varadi, A., Simon, I., and Tusnady, G. E. The BiSearch web server. BMC Bioinform 7, 431, 2006.
22. Carr, I. M., Valleley, E. M., Cordery, S. F., Markham, A. F., and Bonthron, D. T. Sequence analysis and editing for bisulphite genomic sequencing projects. Nucleic Acids Res 35, e79, 2007.
23. Mutskov, V., and Felsenfeld, G. Silencing of transgene transcription precedes methylation of promoter DNA and histone H3 lysine 9. EMBO J 23, 138, 2004.
24. Pinheiro, J., and Bates, D. Mixed-Effects Models in S and S-PLUS. New York: Springer-Verlag, 2000.
25. Mitchell, J. B., McIntosh, K., Zvonic, S., Garrett, S., Floyd, Z. E., Kloster, A., et al. Immunophenotype of human adiposederived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24, 376, 2006.
26. Bukvic, N., Gentile, M., Susca, F., Fanelli, M., Serio, G., Buonadonna, L., et al. Sex chromosome loss, micronuclei, sister chromatid exchange and aging: a study including 16 centenarians. Mutat Res 498, 159, 2001.
27. Li, Q., and Stamatoyannopoulos, J. A. Position independence and proper developmental control of gamma-globin gene expression require both a 5′ locus control region and a downstream sequence element. Mol Cell Biol 14, 6087, 1994.
28. Izadpanah, R., Kaushal, D., Kriedt, C., Tsien, F., Patel, B., Dufour, J., et al. Long-term in vitro expansion alters the biology of adult mesenchymal stem cells. Cancer Res 68, 4229, 2008.
29. Chuah, M. K., Van Damme, A., Zwinnen, H., Goovaerts, I., Vanslembrouck, V., Collen, D., et al. Long-term persistence of human bone marrow stromal cells transduced with factor VIII-retroviral vectors and transient production of therapeutic levels of human factor VIII in nonmyeloablated immunodeficient mice. Hum Gene Ther 11, 729, 2000.
30. Baum, C., Hegewisch-Becker, S., Eckert, H. G., Stocking, C., and Ostertag, W. Novel retroviral vectors for efficient expression of the multidrug resistance (mdr-1) gene in early hematopoietic cells. J Virol 69, 7541, 1995.
31. McInerney, J. M., Nawrocki, J. R., and Lowrey, C. H. Longterm silencing of retroviral vectors is resistant to reversal by trichostatin A and 5-azacytidine. Gene Ther 7, 653, 2000.
32. Lorincz, M. C., Schubeler, D., Goeke, S. C., Walters, M., Groudine, M., and Martin, D. I. Dynamic analysis of proviral induction and de novo methylation: implications for a histone deacetylase-independent, methylation density-dependent mechanism of transcriptional repression. Mol Cell Biol 20, 842, 2000.
33. Yao, S., Sukonnik, T., Kean, T., Bharadwaj, R. R., Pasceri, P., and Ellis, J. Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol Ther 10, 27, 2004.
34. Cherry, S. R., Biniszkiewicz, D., van Parijs, L., Baltimore, D., and Jaenisch, R. Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol Cell Biol 20, 7419, 2000.
35. Pannell, D., Osborne, C. S., Yao, S., Sukonnik, T., Pasceri, P., Karaiskakis, A., et al. Retrovirus vector silencing is de novo methylase independent and marked by a repressive histone code. EMBO J 19, 5884, 2000.
36. Harraghy, N., Gaussin, A., and Mermod, N. Sustained transgene expression using MAR elements. Curr Gene Ther 8, 353, 2008.
37. Recillas-Targa, F., Pikaart, M. J., Burgess-Beusse, B., Bell, A. C., Litt, M. D., West, A. G., et al. Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities. Proc Natl Acad Sci U S A 99, 6883, 2002.
38. Li, C. L., Xiong, D., Stamatoyannopoulos, G., and Emery, D. W. Genomic and functional assays demonstrate reduced gammaretroviral vector genotoxicity associated with use of the cHS4 chromatin insulator. Mol Ther 17, 716, 2009.
39. Yannaki, E., Tubb, J., Aker, M., Stamatoyannopoulos, G., and Emery, D. W. Topological constraints governing the use of the chicken HS4 chromatin insulator in oncoretrovirus vectors. Mol Ther 5, 589, 2002.
40. Yao, S., Osborne, C. S., Bharadwaj, R. R., Pasceri, P., Sukonnik, T., Pannell, D., et al. Retrovirus silencer blocking by the cHS4 insulator is CTCF independent. Nucleic Acids Res 31, 5317, 2003.
41. Goetze, S., Baer, A., Winkelmann, S., Nehlsen, K., Seibler, J., Maass, K., et al. Performance of genomic bordering elements at predefined genomic loci. Mol Cell Biol 25, 2260, 2005.
42. Klehr, D., Maass, K., and Bode, J. Scaffold-attached regions from the human interferon beta domain can be used to enhance the stable expression of genes under the control of various promoters. Biochemistry 30, 1264, 1991.
43. Kurre, P., Morris, J., Thomasson, B., Kohn, D. B., and Kiem, H. P. Scaffold attachment region-containing retrovirus vectors improve long-term proviral expression after transplantation of GFP-modified CD34+ baboon repopulating cells. Blood 102, 3117, 2003.
44. Galbete, J. L., Buceta, M., and Mermod, N. MAR elements regulate the probability of epigenetic switching between active and inactive gene expression. Mol Biosyst 5, 143, 2009.
45. Ramezani, A., Hawley, T. S., and Hawley, R. G. Performanceand safety-enhanced lentiviral vectors containing the human interferon-beta scaffold attachment region and the chicken beta-globin insulator. Blood 101, 4717, 2003.
46. Ellis, J., and Yao, S. Retrovirus silencing and vector design: relevance to normal and cancer stem cells? Curr Gene Ther 5, 367, 2005.
47. Bode, J., Benham, C., Knopp, A., and Mielke, C. Transcriptional augmentation: modulation of gene expression by scaffold/matrix-attached regions (S/MAR elements). Crit Rev Eukaryot Gene Expr 10, 73, 2000.
48. Cai, S., Han, H. J., and Kohwi-Shigematsu, T. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat Genet 34, 42, 2003.
49. Martens, J. H., Verlaan, M., Kalkhoven, E., Dorsman, J. C., and Zantema, A. Scaffold/matrix attachment region elements interact with a p300-scaffold attachment factor A complex and are bound by acetylated nucleosomes. Mol Cell Biol 22, 2598, 2002.