Polyethylene glycol-mediated fusion between primary mouse mesenchymal stem cells and mouse fibroblasts generates hybrid cells with increased proliferation and altered differentiation

Stem Cells and Development

Volumn 15, Issue 6, 2006, Pages 905-919

  Islam, M Q ^a,b   Meirelles, L Da S ^c   Nardi, N B ^c   Magnusson, P ^b   Islam, K ^a,b  

^a LINKÖPING UNIVERSITY HOSPITAL   (Sweden)

^b LINKÖPING UNIVERSITY   (Sweden)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; ALPHA3 INTEGRIN; ALPHA4 INTEGRIN; ATAXIN 1; BETA1 INTEGRIN; CD11B ANTIGEN; CD18 ANTIGEN; CD31 ANTIGEN; CD445R ANTIGEN; CD45 ANTIGEN; CD90.2 ANTIGEN; CELL SURFACE PROTEIN; HERMES ANTIGEN; LEUKOSIALIN; MACROGOL; MICROSOMAL AMINOPEPTIDASE; PROTEIN GR 1; STEM CELL FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ADIPOGENESIS; ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FUSION; CELL IMMORTALIZATION; CELL LINEAGE; CELL PROLIFERATION; CELL STIMULATION; CELL SURFACE; FIBROBLAST; HYBRID CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SOMATIC CELL;

ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL FUSION; CELL LINE; CHROMOSOME MAPPING; CINNAMATES; FIBROBLASTS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HYBRID CELLS; HYGROMYCIN B; KARYOTYPING; MESENCHYMAL STEM CELLS; MICE; OSTEOGENESIS; POLYETHYLENE GLYCOLS;

ANIMALIA;

EID: 33846455082     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2006.15.905     Document Type: Article

References (64)

1. Poulsom R, MR Alison, SJ Forbes and NA Wright. (2002). Adult stem cell plasticity. J Pathol 197:441-456.
2. Czyz J, C Wiese, A Rolletschek, P Blyszczuk, M Cross and AM Wobus. (2003). Potential of embryonic and adult stem cells in vitro. Biol Chem 384:1391-1409.
3. Young HE and AC Black Jr. (2004). Adult stem cells. Anat Rec A 276:75-102.
4. Blau HM, TR Brazelton and JM Weimann. (2001). The evolving concept of a stem cell: entity or function? Cell 105:829-841.
5. Wagers AJ and IL Weissman. (2004). Plasticity of adult stem cells. Cell 116:639-648.
6. Jaiswal N, SE Haynesworth, AI Caplan and SP Bruder. (1997). Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J Cell Biochem 64:295-312.
7. Johnstone B, TM Hering, AI Caplan, VM Goldberg and JU Yoo. (1998). In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238:265-272.
8. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
9. Phinney DG, G Kopen, RL Isaacson and DJ Prockop. (1999). Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J Cell Biochem 72:570-585.
10. Deans RJ and AB Moseley. (2000). Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28:875-884.
11. Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, T Lund, M Blackstad, J Du, S Aldrich, A Lisberg, WC Low, DA Largaespada and CM Verfaillie. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
12. Herzog EL, L Chai and DS Krause. (2003). Plasticity of marrow-derived stem cells. Blood 102:3483-3493.
13. Barry FP and JM Murphy. (2004). Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568-584.
14. Baksh D, L Song and RS Tuan. (2004). Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy. J Cell Mol Med 8:301-316.
15. Javazon EH, KJ Beggs and AW Flake. (2004). Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 32:414-425.
16. Kassem M. (2004). Mesenchymal stem cells: biological characteristics and potential clinical applications. Cloning Stem Cells 6:369-374.
17. Vassilopoulos G, PR Wang and DW Russell. (2003). Transplanted bone marrow regenerates liver by cell fusion. Nature 422:901-904.
18. Wang X, H Willenbring, Y Akkari, Y Torimaru, M Foster, M Al-Dhalimy, E Lagasse, M Finegold, S Olson and M Grompe. (2003). Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422:897-901.
19. Ogle BM, M Cascalho and JL Platt. (2005). Biological implications of cell fusion. Nat Rev Mol Cell Biol 6:567-575.
20. Thorgeirsson SS and JW Grisham. (2006). Hematopoietic cells as hepatocyte stem cells: a critical review of the evidence. Hepatology 43:2-8.
21. Meirelles Lda S and NB Nardi. (2003). Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br J Haematol 123:702-711.
22. Ohmi K, DS Greenberg, KS Rajavel, S Ryazantsev, HH Li and EF Neufeld. (2003). Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. Proc Natl Acad Sci USA 100:1902-1907.
23. Islam MQ, J Ringe, E Reichmann, R Migotti, M Sittinger, L Da S Meirelles, NB Nardi, P Magnusson and K Islam. (2006). Functional characterization of cell hybrids generated by induced fusion of primary porcine mesenchymal stem cells with an immortal murine cell line. Cell Tissue Res 326:123-137.
24. Migeon BR, TR Brown, J Axelman and CJ Migeon. (1981). Studies of the locus for androgen receptor: localization on the human X chromosome and evidence for homology with the Tfm locus in the mouse. Proc Natl Acad Sci USA 78:6339-6343.
25. Jabs EW, SF Wolf and BR Migeon. (1984). Characterization of a cloned DNA sequence that is present at centromeres of all human autosomes and the X chromosome and shows polymorphic variation. Proc Natl Acad Sci USA 81:4884-4888.
26. Trott DA, AP Cuthbert, CM Todd, M Themis and RF Newbold. (1995). Novel use of a selectable fusion gene as an "in-out" marker for studying genetic loss in mammalian cells. Mol Carcinog 12:213-224.
27. Islam MQ and G Levan. (1987). A new fixation procedure for improved quality G-bands in routine cytogenetic work. Hereditas 107:127-130.
28. da Silva Meirelles L, PC Chagastelles and NB Nardi. (2006). Mesenchymal stem cells reside in virtually all postnatal organs and tissues. J Cell Sci 119:2204-2213.
29. Fink T, L Abildtrup, K Fogd, BM Abdallah, M Kassem, P Ebbesen and V Zachar. (2004). Induction of adipocyte-like phenotype in human mesenchymal stem cells by hypoxia. Stem Cells 22:1346-1355.
30. Magnusson P, O Löfman and L Larsson. (1992). Determination of alkaline phosphatase isoenzymes in serum by high-performance liquid chromatography with post-column reaction detection. J Chromatogr 576:79-86.
31. Smith PK, RI Krohn, GT Hermanson, AK Mallia, FH Gartner, MD Provenzano, EK Fujimoto, NM Goeke, BJ Olson and DC Klenk. (1985). Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85.
32. Narisawa S, D Harmey, P Magnusson and JL Millan. (2005). Conserved epitopes in human and mouse tissue-nonspecific alkaline phosphatase. Second report of the ISOBM TD-9 workshop. Tumour Biol 26:113-120.
33. Hoehn H, EM Bryant and GM Martin. (1978). The replicative life spans of euploid hybrids derived from short-lived and long-lived human skin fibroblast cultures. Cytogenet Cell Genet 21:282-295.
34. Ran Q and OM Pereira-Smith. (2000). Genetic approaches to the study of replicative senescence. Exp Gerontol 35:7-13.
35. Bunn CL and GM Tarrant. (1980). Limited lifespan in somatic cell hybrids and cybrids. Exp Cell Res 127:385-396.
36. Morison IM and AE Reeve. (1998). A catalogue of imprinted genes and parent-of-origin effects in humans and animals. Hum Mol Genet 7:1599-1609.
37. Migeon BR, RA Norum and CM Corsaro. (1974). Isolation and analysis of somatic hybrids derived from two human diploid cells. Proc Natl Acad Sci USA 71:937-941.
38. Norwood TH, WR Pendergrass, CA Sprague and GM Martin. (1974). Dominance of the senescent phenotype in heterokaryons between replicative and post-replicative human fibroblast-like cells. Proc Natl Acad Sci USA 71:2231-2235.
39. Matveeva NM, AG Shilov, EM Kaftanovskaya, LP Maximovsky, AI Zhelezova, AN Golubitsa, SI Bayborodin, MM Fokina and OL Serov. (1998). In vitro and in vivo study of pluripotency in intraspecific hybrid cells obtained by fusion of murine embryonic stem cells with splenocytes. Mol Reprod Dev 50:128-138.
40. Matveeva NM, IE Pristyazhnyuk, SA Temirova, AG Menzorov, A Vasilkova, AG Shilov, A Smith and OL Serov. (2005). Unequal segregation of parental chromosomes in embryonic stem cell hybrids. Mol Reprod Dev 71:305-314.
41. Serov O, N Matveeva, S Kuznetsov, E Kaftanovskaya and I Mittmann. (2001). Embryonic hybrid cells: a powerful tool for studying pluripotency and reprogramming of the differentiated cell chromosomes. An Acad Bras Cienc 73:561-568.
42. Medvinsky A and A Smith. (2003). Stem cells: Fusion brings down barriers. Nature 422:823-825.
43. Cowan CA, J Atienza, DA Melton and K Eggan. (2005). Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 309:1369-1373.
44. Tada M, T Tada, L Lefebvre, SC Barton and MA Surani. (1997). Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO J 16:6510-6520.
45. Tada M, A Morizane, H Kimura, H Kawasaki, JF Ainscough, Y Sasai, N Nakatsuji and T Tada. (2003). Pluripotency of reprogrammed somatic genomes in embryonic stem hybrid cells. Dev Dyn 227:504-510.
46. Kimura H, M Tada, S Hatano, M Yamazaki, N Nakatsuji and T Tada. (2002). Chromatin reprogramming of male somatic cell-derived XIST and TSIX in ES hybrid cells. Cytogenet Genome Res 99:106-114.
47. Tada M, Y Takahama, K Abe, N Nakatsuji and T Tada. (2001). Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr Biol 11:1553-1558.
48. Mise N, T Sado, M Tada, S Takada and N Takagi. (1996). Activation of the inactive X chromosome induced by cell fusion between a murine EC and female somatic cell accompanies reproducible changes in the methylation pattern of the Xist gene. Exp Cell Res 223:193-202.
49. Terada N, T Hamazaki, M Oka, M Hoki, DM Mastalerz, Y Nakano, EM Meyer, L Morel, BE Petersen and EW Scott. (2002). Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416:542-545.
50. Ying QL, J Nichols, EP Evans and AG Smith. (2002). Changing potency by spontaneous fusion. Nature 416:545-548.
51. Que J, RM El Oakley, M Salto-Tellez, N Wong, DP de Kleijn, M Teh, L Retnam and SK Lim. (2004). Generation of hybrid cell lines with endothelial potential from spontaneous fusion of adult bone marrow cells with embryonic fibroblast feeder. In Vitro Cell Dev Biol Anim 40:143-149.
52. Majumdar MK, MA Thiede, SE Haynesworth, SP Bruder and SL Gerson. (2000). Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 9:841-848.
53. Dormady SP, O Bashayan, R Dougherty, XM Zhang and RS Basch. (2001). Immortalized multipotential mesenchymal cells and the hematopoietic microenvironment. J Hematother Stem Cell Res 10:125-140.
54. Minguell JJ, A Erices and P Gonget. (2001). Mesenchymal stem cells. Exp Biol Med (Maywood) 226:507-520.
55. Rodic N, MS Rutenberg and N Terada. (2004). Cell fusion and reprogramming: resolving our transdifferences. Trends Mol Med 10:93-96.
56. Zhang S, D Wang, Z Estrov, S Raj, JT Willerson and ET Yeh. (2004). Both cell fusion and transdifferentiation account for the transformation of human peripheral blood CD34-positive cells into cardiomyocytes in vivo. Circulation 110:3803-3807.
57. Willenbring H, AS Bailey, M Foster, Y Akkari, C Dorrell, S Olson, M Finegold, WH Fleming and M Grompe. (2004). Myelomonocytic cells are sufficient for therapeutic cell fusion in liver. Nature Med 10:744-748.
58. Camargo FD, M Finegold and MA Goodell. (2004). Hematopoietic myelomonocytic cells are the major source of hepatocyte fusion partners. J Clin Invest 113:1266-1270.
59. Reinecke H, E Minami, V Poppa and CE Murry. (2004). Evidence for fusion between cardiac and skeletal muscle cells. Circ Res 94:e56-e60.
60. Oh H, SB Bradfute, TD Gallardo, T Nakamura, V Gaussin, Y Mishina, J Pocius, LH Michael, RR Behringer, DJ Garry, ML Entman and MD Schneider. (2003). Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100:12313-12318.
61. Nygren JM, S Jovinge, M Breitbach, P Sawen, W Roll, J Hescheler, J Taneera, BK Fleischmann and SE Jacobsen. (2004). Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nature Med 10:494-501.
62. Alvarez-Dolado M, R Pardal, JM Garcia-Verdugo, JR Fike, HO Lee, K Pfeffer, C Lois, SJ Morrison and A Alvarez-Buylla. (2003). Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968-973.
63. Camargo FD, R Green, Y Capetanaki, KA Jackson and MA Goodell. (2003). Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nature Med 9:1520-1527.
64. Camargo FD, SM Chambers and MA Goodell. (2004). Stem cell plasticity: from transdifferentiation to macrophage fusion. Cell Prolif 37:55-65.