CD45-CD14+CD34+ murine bone marrow low-adherent mesenchymal primitive cells preserve multilineage differentiation potential in long-term in vitro culture

Molecules and Cells

Volumn 31, Issue 6, 2011, Pages 497-507

  Szade, Krzysztof ^a   Zuba Surma, Ewa ^a   Rutkowski, Andrzej J ^a,b   Jozkowicz, Alicja ^a   Dulak, Jozef ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

bone marrow; differentiation; endothelium; expansion; mesenchymal stem cells

Indexed keywords

CD14 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN;

ADHERENT CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CD34 SELECTION; CELL DIFFERENTIATION; CELL EXPANSION; CELL SUBPOPULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN;

ANIMALS; ANTIGENS, CD14; ANTIGENS, CD34; ANTIGENS, CD45; BONE MARROW CELLS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM; GENE EXPRESSION; LECTINS; LIPOPROTEINS, LDL; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONS; PHENOTYPE; PPAR GAMMA; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VON WILLEBRAND FACTOR;

MURINAE;

EID: 79960613393     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-011-2176-y     Document Type: Article

References (44)

1. A. Abdel-Latif R. Bolli I.M. Tleyjeh V.M. Montori E.C. Perin C.A. Hornung E.K. Zuba-Surma M. Al-Mallah B. Dawn 2007 Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis Arch. Intern. Med. 167 989 997 17533201 10.1001/archinte.167.10.989 (Pubitemid 46835786)
2. F. Alviano V. Fossati C. Marchionni M. Arpinati L. Bonsi M. Franchina G. Lanzoni S. Cantoni C. Cavallini F. Bianchi, et al. 2007 Term Amniotic membrane is a high throughput source for multipotent Mesenchymal Stem Cells with the ability to differentiate into endothelial cells in vitro BMC Dev. Biol. 7 11 17313666 10.1186/1471-213X-7-11 (Pubitemid 46371269)
3. N. Beyer Nardi L. da Silva Meirelles 2006 Mesenchymal stem cells: isolation, in vitro expansion and characterization Handb. Exp. Pharmacol. 174 249 282 16370331
4. K.R. Brunt S.R.R. Hall C.A. Ward L.G. Melo 2007 Endothelial progenitor cell and mesenchymal stem cell isolation, characterization, viral transduction Methods Mol. Med. 139 197 210 18287673 10.1007/978-1-59745-571-8-12 1:CAS:528:DC%2BD1cXhtVOnt7nN
5. A. Chawla E.J. Schwarz D.D. Dimaculangan M.A. Lazar 1994 Peroxisome proliferator-activated receptor (PPAR) gamma: adipose-predominant expression and induction early in adipocyte differentiation Endocrinology 135 798 800 8033830 10.1210/en.135.2.798 1:CAS:528:DyaK2cXltVGjtbo%3D (Pubitemid 24241266)
6. M. Chen P. Lie Z. Li X. Wei 2009 Endothelial differentiation of Wharton's jelly-derived mesenchymal stem cells in comparison with bone marrow-derived mesenchymal stem cells Exp. Hematol. 37 629 640 19375653 10.1016/j.exphem.2009. 02.003 1:CAS:528:DC%2BD1MXkslOjtbo%3D
7. O. Cleaver D.A. Melton 2003 Endothelial signaling during development Nat. Med. 9 661 668 12778164 10.1038/nm0603-661 1:CAS:528:DC%2BD3sXktFOntbc%3D (Pubitemid 36749214)
8. I. Copland K. Sharma L. Lejeune N. Eliopoulos D. Stewart P. Liu K. Lachapelle J. Galipeau 2008 CD34 expression on murine marrow-derived mesenchymal stromal cells: impact on neovascularization Exp. Hematol. 36 93 103 18023523 10.1016/j.exphem.2007.08.032 1:CAS:528:DC%2BD2sXhsVOrtr3N (Pubitemid 350266974)
9. B. Dawn S. Tiwari M.J. Kucia E.K. Zuba-Surma Y. Guo S.K. Sanganalmath A. Abdel-Latif G. Hunt R.J. Vincent H. Taher, et al. 2008 Transplantation of bone marrow-derived very small embryonic-like stem cells attenuates left ventricular dysfunction and remodeling after myocardial infarction Stem Cells 26 1646 1655 18420834 10.1634/stemcells.2007-0715
10. B. Dawn A. Abdel-Latif S.K. Sanganalmath M.P. Flaherty E.K. Zuba-Surma 2009 Cardiac repair with adult bone marrowderived cells: the clinical evidence Antioxid. Redox Signal. 11 1865 1882 19203221 10.1089/ars.2009.2462 1:CAS:528:DC%2BD1MXotVentbw%3D
11. G. D'Ippolito S. Diabira G.A. Howard P. Menei B.A. Roos P.C. Schiller 2004 Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential J. Cell Sci. 117 2971 2981 15173316 10.1242/jcs.01103 (Pubitemid 39117672)
12. R.G. Fei P.E. Penn N.S. Wolf 1990 A method to establish pure fibroblast and endothelial cell colony cultures from murine bone marrow Exp. Hematol. 18 953 957 2201558 1:STN:280:DyaK3czltlCkuw%3D%3D (Pubitemid 20300987)
13. B. Fernandez Pujol F.C. Lucibello U.M. Gehling K. Lindemann N. Weidner M.L. Zuzarte J. Adamkiewicz H.P. Elsässer R. Müller K. Havemann 2000 Endothelial-like cells derived from human CD14 positive monocytes Differentiation 65 287 300 10929208 10.1046/j.1432-0436.2000.6550287.x 1:STN:280:DC%2BD3M%2FivFCnuw%3D%3D (Pubitemid 30406634)
14. E.J. Gang J.A. Jeong S. Han Q. Yan C. Jeon H. Kim 2006 In vitro endothelial potential of human UC blood-derived mesenchymal stem cells Cytotherapy 8 215 227 16793731 10.1080/14653240600735933 1:STN:280: DC%2BD28znslOnsA%3D%3D (Pubitemid 43947788)
15. Girdlestone, J., Limbani, V., Cutler, A., and Navarrete, C. (2009). Efficient expansion of mesenchymal stromal cells from umbilical cord under low serum conditions. Cytotherapy [Epub ahead of print].
16. M. Gnecchi L.G. Melo 2009 Bone marrow-derived mesenchymal stem cells: isolation, expansion, characterization, viral transduction, and production of conditioned medium Methods Mol. Biol. 482 281 294 19089363 10.1007/978-1-59745- 060-7-18 1:CAS:528:DC%2BD1MXhslWgs78%3D
17. J.E. Grove E. Bruscia D.S. Krause 2004 Plasticity of bone marrow-derived stem cells Stem Cells 22 487 500 15277695 10.1634/stemcells.22-4-487 (Pubitemid 39014565)
18. C.P. Hofstetter E.J. Schwarz D. Hess J. Widenfalk A. El Manira D.J. Prockop L. Olson 2002 Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery Proc. Natl. Acad. Sci. USA 99 2199 2204 11854516 10.1073/pnas.042678299 1:CAS:528:DC%2BD38XitVSrtL8%3D (Pubitemid 34169038)
19. D.D. Houlihan P.N. Newsome 2008 Critical review of clinical trials of bone marrow stem cells in liver disease Gastroenterology 135 438 450 18585384 10.1053/j.gastro.2008.05.040 1:CAS:528:DC%2BD1cXhtVCqsL%2FI
20. D.A. Ingram L.E. Mead H. Tanaka V. Meade A. Fenoglio K. Mortell K. Pollok M.J. Ferkowicz D. Gilley M.C. Yoder 2004 Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood Blood 104 2752 2760 15226175 10.1182/blood-2004-04-1396 1:CAS:528: DC%2BD2cXpslKjtrg%3D (Pubitemid 39434958)
21. R.K. Jain 2003 Molecular regulation of vessel maturation Nat. Med. 9 685 693 12778167 10.1038/nm0603-685 1:CAS:528:DC%2BD3sXktFOnurw%3D (Pubitemid 36749217)
22. Y. Jiang B.N. Jahagirdar R.L. Reinhardt R.E. Schwartz C.D. Keene X.R. Ortiz-Gonzalez M. Reyes T. Lenvik T. Lund M. Blackstad, et al. 2002 Pluripotency of mesenchymal stem cells derived from adult marrow Nature 418 41 49 12077603 10.1038/nature00870 1:CAS:528:DC%2BD38XltVantrs%3D (Pubitemid 34742565)
23. P. Kabos M. Ehtesham A. Kabosova K.L. Black J.S. Yu 2002 Generation of neural progenitor cells from whole adult bone marrow Exp. Neurol. 178 288 293 12504887 10.1006/exnr.2002.8039 1:CAS:528:DC%2BD38Xps12kurg%3D (Pubitemid 36062638)
24. S. Kaiser B. Hackanson M. Follo A. Mehlhorn K. Geiger G. Ihorst U. Kapp 2007 BM cells giving rise to MSC in culture have a heterogeneous CD34 and CD45 phenotype Cytotherapy 9 439 450 17786605 10.1080/14653240701358445 1:CAS:528:DC%2BD2sXhtVSksbzN (Pubitemid 47386681)
25. D. Karussis I. Kassis B.G.S. Kurkalli S. Slavin 2008 Immunomodulation and neuroprotection with mesenchymal bone marrow stem cells (MSCs): a proposed treatment for multiple sclerosis and other neuroimmunological/neurodegenerative diseases J. Neurol. Sci. 265 131 135 17610906 10.1016/j.jns.2007.05.005 1:CAS:528:DC%2BD1cXlsVWmuw%3D%3D
26. R.A. Kopher V.R. Penchev M.S. Islam K.L. Hill S. Khosla D.S. Kaufman 2010 Human embryonic stem cell-derived CD34+ cells function as MSC progenitor cells Bone 47 718 728 20601304 10.1016/j.bone.2010.06.020 1:CAS:528:DC%2BC3cXhtFClsb3M
27. M. Kucia R. Reca F.R. Campbell E. Zuba-Surma M. Majka J. Ratajczak M.Z. Ratajczak 2006 A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow Leukemia 20 857 869 16498386 10.1038/sj.leu.2404171 1:CAS:528:DC%2BD28XjslOhtbY%3D
28. M. Kucia M. Wysoczynski J. Ratajczak M.Z. Ratajczak 2008 Identification of very small embryonic like (VSEL) stem cells in bone marrow Cell Tissue Res. 331 125 134 17828555 10.1007/s00441-007-0485-4 1:STN:280:DC%2BD2sjjslylsA%3D%3D (Pubitemid 350265493)
29. M. Kuwana Y. Okazaki H. Kodama K. Izumi H. Yasuoka Y. Ogawa Y. Kawakami Y. Ikeda 2003 Human circulating CD14+ monocytes as a source of progenitors that exhibit mesenchymal cell differentiation J. Leukoc. Biol. 74 833 845 12960274 10.1189/jlb.0403170 1:CAS:528:DC%2BD3sXpt1CrtLs%3D (Pubitemid 38040360)
30. Y. Li C. Zhang F. Xiong M. Yu F. Peng Y. Shang C. Zhao Y. Xu Z. Liu C. Zhou, et al. 2008 Comparative study of mesenchymal stem cells from C57BL/10 and mdx mice BMC Cell Biol. 9 24 18489762 10.1186/1471-2121-9-24 (Pubitemid 351803886)
31. S.Y. Lim Y.S. Kim Y. Ahn M.H. Jeong M.H. Hong S.Y. Joo K.I. Nam J.G. Cho P.M. Kang J.C. Park 2006 The effects of mesenchymal stem cells transduced with Akt in a porcine myocardial infarction model Cardiovasc. Res. 70 530 542 16563361 10.1016/j.cardiores.2006.02.016 1:CAS:528:DC%2BD28Xks1Wlu78%3D (Pubitemid 43732376)
32. E. Martin-Rendon S.J. Brunskill C.J. Hyde S.J. Stanworth A. Mathur S.M. Watt 2008 Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review Eur. Heart J. 29 1807 1818 18523058 10.1093/eurheartj/ehn220 1:CAS:528:DC%2BD1cXhtVGmtbfO
33. S. Matoba T. Tatsumi T. Murohara T. Imaizumi Y. Katsuda M. Ito Y. Saito S. Uemura H. Suzuki S. Fukumoto, et al. 2008 Long-term clinical outcome after intramuscular implantation of bone marrow mononuclear cells (therapeutic angiogenesis by cell transplantation [TACT] trial) in patients with chronic limb ischemia Am. Heart J. 156 1010 1018 19061721 10.1016/j.ahj.2008.06.025
34. J. Oswald S. Boxberger B. Jørgensen S. Feldmann G. Ehninger M. Bornhäuser C. Werner 2004 Mesenchymal stem cells can be differentiated into endothelial cells in vitro Stem Cells 22 377 384 15153614 10.1634/stemcells.22- 3-377 (Pubitemid 38736621)
35. D.G. Phinney D.J. Prockop 2007 Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views Stem Cells 25 2896 2902 17901396 10.1634/stemcells.2007-0637 (Pubitemid 350127874)
36. R.E. Pitas J. Boyles R.W. Mahley D.M. Bissell 1985 Uptake of chemically modified low density lipoproteins in vivo is mediated by specific endothelial cells J. Cell Biol. 100 103 117 3965468 10.1083/jcb.100.1.103 1:CAS:528:DyaL2MXns1ejsQ%3D%3D (Pubitemid 15151886)
37. M.F. Pittenger A.M. Mackay S.C. Beck R.K. Jaiswal R. Douglas J.D. Mosca M.A. Moorman D.W. Simonetti S. Craig D.R. Marshak 1999 Multilineage potential of adult human mesenchymal stem cells Science 284 143 147 10102814 10.1126/science.284.5411.143 1:CAS:528:DyaK1MXitlCnu7o%3D (Pubitemid 29282067)
38. N. Quirici D. Soligo L. Caneva F. Servida P. Bossolasco G.L. Deliliers 2001 Differentiation and expansion of endothelial cells from human bone marrow CD133(+) cells Br. J. Haematol. 115 186 94 11722432 10.1046/j.1365-2141.2001. 03077.x 1:CAS:528:DC%2BD3MXotFWmtrg%3D (Pubitemid 32995115)
39. B.A. Reynolds S. Weiss 1992 Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science 255 1707 1710 1553558 10.1126/science.1553558 1:STN:280:DyaK383gsFemsw%3D%3D
40. P. Romagnani F. Annunziato F. Liotta E. Lazzeri B. Mazzinghi F. Frosali L. Cosmi L. Maggi L. Lasagni A. Scheffold, et al. 2005 CD14+CD34 low cells with stem cell phenotypic and functional features are the major source of circulating endothelial progenitors Circ. Res. 97 314 322 16020753 10.1161/01.RES. 0000177670.72216.9b 1:CAS:528:DC%2BD2MXntlSitbY%3D (Pubitemid 41216135)
41. M. Shiota T. Heike M. Haruyama S. Baba A. Tsuchiya H. Fujino H. Kobayashi T. Kato K. Umeda M. Yoshimoto, et al. 2007 Isolation and characterization of bone marrow-derived mesenchymal progenitor cells with myogenic and neuronal properties Exp. Cell Res. 313 1008 1023 17289022 10.1016/j.yexcr.2006.12.017 1:CAS:528:DC%2BD2sXit12isL0%3D (Pubitemid 46273446)
42. Y. Torrente E. Polli 2008 Mesenchymal stem cell transplantation for neurodegenerative diseases Cell Transplant 17 1103 1113 19181205 10.3727/096368908787236576
43. Q.R. Wang B.H. Wang Y.H. Huang G. Dai W.M. Li Q. Yan 2008 Purification and growth of endothelial progenitor cells from murine bone marrow mononuclear cells J. Cell Biochem. 103 21 29 17471503 10.1002/jcb.21377 1:CAS:528: DC%2BD1cXnsVGgsQ%3D%3D
44. S.J. Zhang H. Zhang M. Hou Z. Zheng J. Zhou W. Su Y. Wei S. Hu 2007 Is it possible to obtain "true endothelial progenitor cells" by in vitro culture of bone marrow mononuclear cells? Stem Cells Dev 16 683 690 17784841 10.1089/scd.2006.0062 1:CAS:528:DC%2BD2sXpvFWrsbs%3D (Pubitemid 47378740)