Sustained and promoter dependent bone morphogenetic protein expression by rat mesenchymal stem cells after BMP-2 transgene electrotransfer

European Cells and Materials

Volumn 24, Issue , 2012, Pages 18-28

  Ferreira, Elisabeth ^a,b   Potier, Esther ^a,c   Vaudin, Pascal ^d,e   Oudina, Karim ^a   Bensidhoum, Morad ^a   Logeart Avramoglou, Delphine ^a   Mir, Lluis M ^f,g   Petite, Hervé ^a  

^a Paris university   (France)

^b HARVARD MEDICAL SCHOOL   (United States)

^c EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d INSERM   (France)

^e UNIVERSITÉ DE TOURS   (France)

^f INSTITUT GUSTAVE ROUSSY   (France)

^g UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Bone morphogenetic proteins; Electroporation; Gene delivery; Marrow stromal cells; Mesenchymal stem cells; Promoter activity

Indexed keywords

BETA ACTIN; BONE MORPHOGENETIC PROTEIN 2; ELONGATION FACTOR 1ALPHA; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; OSTEOCALCIN;

ANIMAL CELL; ARTICLE; BONE MORPHOGENETIC PROTEIN 2 GENE; CELL DIFFERENTIATION; CYTOMEGALOVIRUS; ELECTROPORATION; GENE DOSAGE; GENE EXPRESSION; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN SECRETION; RAT; SAFETY; TRANSGENE;

EID: 84864047833     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v024a02     Document Type: Article

References (46)

1. Aslan H, Zilberman Y, Arbeli V, Sheyn D, Matan Y, Liebergall M, Li JZ, Helm GA, Gazit D, Gazit Z (2006) Nucleofection-based ex vivo nonviral gene delivery to human stem cells as a platform for tissue regeneration. Tissue Eng 12: 877-889.
2. Baltzer AW, Lattermann C, Whalen JD, Wooley P, Weiss K, Grimm M, Ghivizzani SC, Robbins PD, Evans CH (2000) Genetic enhancement of fracture repair: healing of an experimental segmental defect by adenoviral transfer of the BMP-2 gene. Gene Ther 7: 734-739.
3. Bensidhoum M, Chapel A, Francois S, Demarquay C, Mazurier C, Fouillard L, Bouchet S, Bertho JM, Gourmelon P, Aigueperse J, Charbord P, Gorin NC, Thierry D, Lopez M (2004) Homing of in vitro expanded Stro-1-or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34 cell engraftment. Blood 103: 3313-3319.
4. Birkholz K, Hombach A, Krug C, Reuter S, Kershaw M, Kampgen E, Schuler G, Abken H, Schaft N, Dorrie J (2009) Transfer of mRNA encoding recombinant immunoreceptors reprograms CD4(+) and CD8(+) T cells for use in the adoptive immunotherapy of cancer. Gene Ther 16: 596-604.
5. Blum JS, Barry MA, Mikos AG, Jansen JA (2003) In vivo evaluation of gene therapy vectors in ex vivo-derived marrow stromal cells for bone regeneration in a rat critical-size calvarial defect model. Hum Gene Ther 14: 1689-1701.
6. Byun HM, Suh D, Jeong Y, Wee HS, Kim JM, Kim WK, Ko JJ, Kim JS, Lee YB, Oh YK (2005) Plasmid vectors harboring cellular promoters can induce prolonged gene expression in hematopoietic and mesenchymal progenitor cells. Biochem Biophys Res Commun 332: 518-523.
7. Choi JY, Lee BH, Song KB, Park RW, Kim IS, Sohn KY, Jo JS, Ryoo HM (1996) Expression patterns of bone-related proteins during osteoblastic differentiation in MC3T3-E1 cells. J Cell Biochem 61: 609-618.
8. Chuang CK, Sung LY, Hwang SM, Lo WH, Chen HC, Hu YC (2007) Baculovirus as a new gene delivery vector for stem cell engineering and bone tissue engineering. Gene Ther 14: 1417-1424.
9. Daud AI, DeConti RC, Andrews S, Urbas P, Riker AI, Sondak VK, Munster PN, Sullivan DM, Ugen KE, Messina JL, Heller R (2008) Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 26: 5896-5903.
10. Doll RF, Crandall JE, Dyer CA, Aucoin JM, Smith FI (1996) Comparison of promoter strengths on gene delivery into mammalian brain cells using AAV vectors. Gene Ther 3: 437-447.
11. Duces A, Karaky R, Martel-Renoir D, Mir L, Hamma-Kourbali Y, Bieche I, Opolon P, Delbe J, Courty J, Perricaudet M, Griscelli F (2008) 16-kDa fragment of pleiotrophin acts on endothelial and breast tumor cells and inhibits tumor development. Mol Cancer Ther 7: 2817-2827.
12. Durieux AC, Bonnefoy R, Freyssenet D (2005) Kinetic of transgene expression after electrotransfer into skeletal muscle: importance of promoter origin/strength. Biochim Biophys Acta 1725: 403-409.
13. Ercolani L, Florence B, Denaro M, Alexander M (1988) Isolation and complete sequence of a functional human glyceraldehyde-3-phosphate dehydrogenase gene. J Biol Chem 263: 15335-15341.
14. Feeley BT, Conduah AH, Sugiyama O, Krenek L, Chen IS, Lieberman JR (2006) In vivo molecular imaging of adenoviral versus lentiviral gene therapy in two bone formation models. J Orthop Res 24: 1709-1721.
15. Ferreira E, Potier E, Logeart-Avramoglou D, Salomskaite-Davalgiene S, Mir LM, Petite H (2008) Optimization of a gene electrotransfer method for mesenchymal stem cell transfection. Gene Ther 15: 537-544.
16. Friedenstein AJ, Chailakhjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3: 393-403.
17. Gill DR, Smyth SE, Goddard CA, Pringle IA, Higgins CF, Colledge WH, Hyde SC (2001) Increased persistence of lung gene expression using plasmids containing the ubiquitin C or elongation factor 1alpha promoter. Gene Ther 8: 1539-1546.
18. Graven KK, Yu Q, Pan D, Roncarati JS, Farber HW (1999) Identification of an oxygen responsive enhancer element in the glyceraldehyde-3-phosphate dehydrogenase gene. Biochim Biophys Acta 1447: 208-218.
19. Hong S, Hwang DY, Yoon S, Isacson O, Ramezani A, Hawley RG, Kim KS (2007) Functional analysis of various promoters in lentiviral vectors at different stages of in vitro differentiation of mouse embryonic stem cells. Mol Ther 15: 1630-1639.
20. Hou Z, Nguyen Q, Frenkel B, Nilsson SK, Milne M, van Wijnen AJ, Stein JL, Quesenberry P, Lian JB, Stein GS (1999) Osteoblast-specific gene expression after transplantation of marrow cells: implications for skeletal gene therapy. Proc Natl Acad Sci USA 96: 7294-7299.
21. Hsu WK, Sugiyama O, Park SH, Conduah A, Feeley BT, Liu NQ, Krenek L, Virk MS, An DS, Chen IS, Lieberman JR (2007) Lentiviral-mediated BMP-2 gene transfer enhances healing of segmental femoral defects in rats. Bone 40: 931-938.
22. Kumar S, Mahendra G, Ponnazhagan S (2005) Determination of osteoprogenitor-specific promoter activity in mouse mesenchymal stem cells by recombinant adeno-associated virus transduction. Biochim Biophys Acta 1731: 95-103.
23. Lieberman JR, Le LQ, Wu L, Finerman GA, Berk A, Witte ON, Stevenson S (1998) Regional gene therapy with a BMP-2-producing murine stromal cell line induces heterotopic and orthotopic bone formation in rodents. J Orthop Res 16: 330-339.
24. Lou J, Xu F, Merkel K, Manske P (1999) Gene therapy: adenovirus-mediated human bone morphogenetic protein-2 gene transfer induces mesenchymal progenitor cell proliferation and differentiation in vitro and bone formation in vivo. J Orthop Res 17: 43-50.
25. Lu K, Zeng D, Zhang W, Xia L, Xu L, Jiang X, Zhang F (2012) Ectopic study of calcium phosphate cement seeded with pBMP-2 modified canine bMSCs mediated by a non-viral PEI derivative. Cell Biol Int 36: 119-128.
26. Malaval L, Modrowski D, Gupta AK, Aubin JE (1994) Cellular expression of bone-related proteins during in vitro osteogenesis in rat bone marrow stromal cell cultures. J Cell Physiol 158: 555-572.
27. McMahon JM, Conroy S, Lyons M, Greiser U, O'Shea C, Strappe P, Howard L, Murphy M, Barry F, O'Brien T (2006) Gene transfer into rat mesenchymal stem cells: a comparative study of viral and nonviral vectors. Stem Cells Dev 15: 87-96.
28. Musgrave DS, Bosch P, Lee JY, Pelinkovic D, Ghivizzani SC, Whalen J, Niyibizi C, Huard J (2000) Ex vivo gene therapy to produce bone using different cell types. Clin Orthop Relat Res 378: 290-305.
29. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH (1982) Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1: 841-845.
30. Olmsted-Davis EA, Gugala Z, Gannon FH, Yotnda P, McAlhany RE, Lindsey RW, Davis AR (2002) Use of a chimeric adenovirus vector enhances BMP2 production and bone formation. Hum Gene Ther 13: 1337-1347.
31. Parham JH, Iannone MA, Overton LK, Hutchins JT (1998) Optimization of transient gene expression in mammalian cells and potential for scale-up using flow electroporation. Cytotechnology 28: 147-155.
32. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
33. Pucihar G, Mir LM, Miklavcic D (2002) The effect of pulse repetition frequency on the uptake into electropermeabilized cells in vitro with possible applications in electrochemotherapy. Bioelectrochemistry 57: 167-172.
34. Quinn CM, Wiles AP, El-Shanawany T, Catchpole I, Alnadaf T, Ford MJ, Gordon S, Greaves DR (1999) The human eukaryotic initiation factor 4AI gene (EIF4A1) contains multiple regulatory elements that direct high-level reporter gene expression in mammalian cell lines. Genomics 62: 468-476.
35. Ramezani A, Hawley TS, Hawley RG (2000) Lentiviral vectors for enhanced gene expression in human hematopoietic cells. Mol Ther 2: 458-469.
36. Sakurai F, Kawabata K, Yamaguchi T, Hayakawa T, Mizuguchi H (2005) Optimization of adenovirus serotype 35 vectors for efficient transduction in human hematopoietic progenitors: comparison of promoter activities. Gene Ther 12: 1424-1433.
37. Spenger A, Ernst W, Condreay JP, Kost TA, Grabherr R (2004) Influence of promoter choice and trichostatin A treatment on expression of baculovirus delivered genes in mammalian cells. Protein Expr Purif 38: 17-23.
38. Sugiyama H, Niwa H, Makino K, Kakunaga T (1988) Strong transcriptional promoter in the 5' upstream region of the human beta-actin gene. Gene 65: 135-139.
39. Sugiyama O, An DS, Kung SP, Feeley BT, Gamradt S, Liu NQ, Chen IS, Lieberman JR (2005) Lentivirus-mediated gene transfer induces long-term transgene expression of BMP-2 in vitro and new bone formation in vivo. Mol Ther 11: 390-398.
40. Suzuki M, Oda E, Nakajima T, Sekiya S, Oda K (1998) Induction of Sp1 in differentiating human embryonal carcinoma cells triggers transcription of the fibronectin gene. Mol Cell Biol 18: 3010-3020.
41. Tsuchida H, Hashimoto J, Crawford E, Manske P, Lou J (2003) Engineered allogeneic mesenchymal stem cells repair femoral segmental defect in rats. J Orthop Res 21: 44-53.
42. Urist MR, Mikulski A, Lietze A (1979) Solubilized and insolubilized bone morphogenetic protein. Proc Natl Acad Sci USA 76: 1828-1832.
43. Wegman F, Bijenhof A, Schuijff L, Oner FC, Dhert WJ, Alblas J (2011) Osteogenic differentiation as a result of BMP-2 plasmid DNA based gene therapy in vitro and in vivo. Eur Cell Mater 21: 230-242.
44. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA (1988) Novel regulators of bone formation: molecular clones and activities. Science 242: 1528-1534.
45. Wu MH, Smith SL, Dolan ME (2001) High efficiency electroporation of human umbilical cord blood CD34+ hematopoietic precursor cells. Stem Cells 19: 492-499.
46. Zhao B, Katagiri T, Toyoda H, Takada T, Yanai T, Fukuda T, Chung UI, Koike T, Takaoka K, Kamijo R (2006) Heparin potentiates the in vivo ectopic bone formation induced by bone morphogenetic protein-2. J Biol Chem 281: 23246-23253.