Distinct in vitro properties of embryonic and extraembryonic fibroblast-like cells are reflected in their in vivo behavior following grafting in the adult mouse brain

Cell Transplantation

Volumn 24, Issue 2, 2015, Pages 223-233

  Costa, Roberta ^a   Bergwerf, Irene ^b   Santermans, Eva ^c   De Vocht, Nathalie ^b   Praet, Jelle ^b   Daans, Jasmijn ^b   Le Blon, Debbie ^b   Hoornaert, Chloé ^b   Reekmans, Kristien ^b   Hens, Niel ^b,c   Goossens, Herman ^b   Berneman, Zwi ^b   Parolini, Ornella ^d   Alviano, Francesco ^a   Ponsaerts, Peter ^b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c HASSELT UNIVERSITY   (Belgium)

^d Fondazione Poliambulanza Istituto Ospedaliero   (Italy)

Author keywords

Angiogenesis; Brain; Embryonic fibroblasts; Fetal membrane derived stromal cells; Immunomodulation; Transplantation

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN GRAFT; CELL DIFFERENTIATION; CELL FUNCTION; CELL TRANSPLANTATION; DOWN REGULATION; EMBRYO; FEMALE; FIBROBLAST; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MACROGLIA; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; STROMA CELL; ALLOTRANSPLANTATION; ANIMAL; ANIMAL EMBRYO; BRAIN; C57BL MOUSE; CELL CULTURE; COCULTURE; CYTOLOGY; DRUG EFFECTS; EMBRYO MEMBRANE; IMMUNOPHENOTYPING; METABOLISM; PATHOLOGY; TRANSPLANTATION;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYO, MAMMALIAN; EXTRAEMBRYONIC MEMBRANES; FEMALE; FIBROBLASTS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICROGLIA; STROMAL CELLS; TRANSPLANTATION, HOMOLOGOUS; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84923200638     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368913X676196     Document Type: Article

References (30)

1. Atoui, R.; Chiu, R. C. Concise review: Immunomodulatory properties of mesenchymal stem cells in cellular transplantation: Update, controversies, and unknowns. Stem Cells Transl. Med. 1(3):200-205; 2012.
2. Barry, F. P.; Murphy, J. M. Mesenchymal stem cells: Clinical applications and biological characterization. Int. J. Biochem. Cell Biol. 36(4):568-584; 2004.
3. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate-A practical and powerful approach to multiple testing. J. R. Statist. Soc. B. 57(1):289-300; 1995.
4. Bergwerf, I.; De Vocht, N.; Tambuyzer, B.; Verschueren, J.; Reekmans, K.; Daans, J.; Ibrahimi, A.; Van Tendeloo, V.; Chatterjee, S.; Goossens, H.; Jorens, P. G.; Baekelandt, V.; Ysebaert, D.; Van Marck, E.; Berneman, Z. N.; Van der Linden, A.; Ponsaerts, P. Reporter gene-expressing bone marrow-derived stromal cells are immune-tolerated following implantation in the central nervous system of syngeneic immunocompetent mice. BMC Biotechnol. 9:1; 2009.
5. Bergwerf, I.; Tambuyzer, B.; De Vocht, N.; Reekmans, K.; Praet, J.; Daans, J.; Chatterjee, S.; Pauwels, P.; Van der Linden, A.; Berneman, Z. N.; Ponsaerts, P. Recognition of cellular implants by the brain’s innate immune system. Immunol. Cell Biol. 89(4):511-516; 2011.
6. Bidarra, S. J.; Barrias, C. C.; Barbosa, M. A.; Soares, R.; Amedee, J.; Granja, P. L. Phenotypic and proliferative modulation of human mesenchymal stem cells via crosstalk with endothelial cells. Stem Cell Res. 7(3):186-197; 2011.
7. Bieback, K.; Wuchter, P.; Besser, D.; Franke, W.; Becker, M.; Ott, M.; Pacher, M.; Ma, N.; Stamm, C.; Kluter, H.; Muller, A.; Ho, A. D. Mesenchymal stromal cells (MSCs): Science and f(r)iction. J. Mol. Med. 90(7):773-782; 2012.
8. Cargnoni, A.; Gibelli, L.; Tosini, A.; Signoroni, P. B.; Nassuato, C.; Arienti, D.; Lombardi, G.; Albertini, A.; Wengler, G. S.; Parolini, O. Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycininduced lung fibrosis. Cell Transplant. 18(4):405-422; 2009.
9. Dailey, T.; Tajiri, N.; Kaneko, Y.; Borlongan, C. V. Regeneration of neuronal cells following cerebral injury. Front. Neurol. Neurosci. 32:54-61; 2013.
10. De Vocht, N.; Lin, D.; Praet, J.; Hoornaert, C.; Reekmans, K.; Le Blon, D.; Daans, J.; Pauwels, P.; Goossens, H.; Hens, N.; Berneman, Z.; Van der Linden, A.; Ponsaerts, P. Quantitative and phenotypic analysis of mesenchymal stromal cell graft survival and recognition by microglia and astrocytes in mouse brain. Immunobiology 218(5):696-705; 2013.
11. Dobreva, M. P.; Pereira, P. N.; Deprest, J.; Zwijsen, A. On the origin of amniotic stem cells: Of mice and men. Int. J. Dev. Biol. 54(5):761-777; 2010.
12. Evangelista, M.; Soncini, M.; Parolini, O. Placenta-derived stem cells: New hope for cell therapy? Cytotechnology 58(1): 33-42; 2008.
13. Haniffa, M. A.; Collin, M. P.; Buckley, C. D.; Dazzi, F. Mesenchymal stem cells: The fibroblasts’ new clothes? Haematologica 94(2):258-263; 2009.
14. Ilancheran, S.; Moodley, Y.; Manuelpillai, U. Human fetal membranes: A source of stem cells for tissue regeneration and repair? Placenta 30(1):2-10; 2009.
15. Liu, K. J.; Wang, C. J.; Chang, C. J.; Hu, H. I.; Hsu, P. J.; Wu, Y. C.; Bai, C. H.; Sytwu, H. K.; Yen, B. L. Surface expression of HLA-G is involved in mediating immunomodulatory effects of placenta-derived multipotent cells (PDMCs) towards natural killer lymphocytes. Cell Transplant. 20(11-12):1721-1730; 2011.
16. Manuelpillai, U.; Moodley, Y.; Borlongan, C. V.; Parolini, O. Amniotic membrane and amniotic cells: Potential therapeutic tools to combat tissue inflammation and fibrosis? Placenta 32(Suppl 4):S320-S325; 2011.
17. Manuelpillai, U.; Tchongue, J.; Lourensz, D.; Vaghjiani, V.; Samuel, C. S.; Liu, A.; Williams, E. D.; Sievert, W. Transplantation of human amnion epithelial cells reduces hepatic fibrosis in immunocompetent CCl(4)-treated mice. Cell Transplant. 19(9):1157-1168; 2010.
18. Oskowitz, A.; McFerrin, H.; Gutschow, M.; Carter, M. L.; Pochampally, R. Serum-deprived human multipotent mesenchymal stromal cells (MSCs) are highly angiogenic. Stem Cell Res. 6(3):215-225; 2011.
19. Parolini, O.; Alviano, F.; Bergwerf, I.; Boraschi, D.; De Bari, C.; De Waele, P.; Dominici, M.; Evangelista, M.; Falk, W.; Hennerbichler, S.; Hess, D. C.; Lanzoni, G.; Liu, B.; Marongiu, F.; McGuckin, C.; Mohr, S.; Nolli, M. L.; Ofir, R.; Ponsaerts, P.; Romagnoli, L.; Solomon, A.; Soncini, M.; Strom, S.; Surbek, D.; Venkatachalam, S.; Wolbank, S.; Zeisberger, S.; Zeitlin, A.; Zisch, A.; Borlongan, C. V. Toward cell therapy using placenta-derived cells: Disease mechanisms, cell biology, preclinical studies, and regulatory aspects at the round table. Stem Cells Dev. 19(2):143-154; 2010.
20. Payne, N. L.; Sun, G.; McDonald, C.; Layton, D.; Moussa, L.; Emerson-Webber, A.; Veron, N.; Siatskas, C.; Herszfeld, D.; Price, J.; Bernard, C. C. Distinct immunomodulatory and migratory mechanisms underpin the therapeutic potential of human mesenchymal stem cells in autoimmune demyelination. Cell Transplant. 22(8):1409-1425; 2013.
21. Praet, J.; Reekmans, K.; Lin, D.; De Vocht, N.; Bergwerf, I.; Tambuyzer, B.; Daans, J.; Hens, N.; Goossens, H.; Pauwels, P.; Berneman, Z.; Van der Linden, A.; Ponsaerts, P. Cell type-associated differences in migration, survival, and immunogenicity following grafting in CNS tissue. Cell Transplant. 21(9):1867-1881; 2012.
22. Praet, J.; Santermans, E.; Reekmans, K.; de Vocht, N.; Le Blon, D.; Hoornaert, C.; Daans, J.; Goossens, H.; Berneman, Z.; Hens, N.; Van der Linden, A.; Ponsaerts, P. Histological characterization and quantification of cellular events following neural and fibroblast(-like) stem cell grafting in healthy and demyelinated CNS tissue. Methods Mol. Biol. 1213: 265-283; 2014.
23. Reekmans, K.; De Vocht, N.; Praet, J.; Le Blon, D.; Hoornaert, C.; Daans, J.; Van der Linden, A.; Berneman, Z.; Ponsaerts, P. Quantitative evaluation of stem cell grafting in the central nervous system of mice by in vivo bioluminescence imaging and postmortem multicolor histological analysis. Methods Mol. Biol. 1052:125-141; 2013.
24. Reekmans, K.; Praet, J.; Daans, J.; Reumers, V.; Pauwels, P.; Van der Linden, A.; Berneman, Z. N.; Ponsaerts, P. Current challenges for the advancement of neural stem cell biology and transplantation research. Stem Cell Rev. 8(1):262-278; 2012.
25. Ronsyn, M. W.; Berneman, Z. N.; Van Tendeloo, V. F.; Jorens, P. G.; Ponsaerts, P. Can cell therapy heal a spinal cord injury? Spinal Cord 46(8):532-539; 2008.
26. Ronsyn, M. W.; Daans, J.; Spaepen, G.; Chatterjee, S.; Vermeulen, K.; D’Haese, P.; Van Tendeloo, V. F.; Van Marck, E.; Ysebaert, D.; Berneman, Z. N.; Jorens, P. G.; Ponsaerts, P. Plasmid-based genetic modification of human bone marrow-derived stromal cells: Analysis of cell survival and transgene expression after transplantation in rat spinal cord. BMC Biotechnol. 7:90; 2007.
27. Shinozuka, K.; Dailey, T.; Tajiri, N.; Ishikawa, H.; Kim, D. W.; Pabon, M.; Acosta, S.; Kaneko, Y.; Borlongan, C. V. Stem cells for neurovascular repair in stroke. J. Stem Cell Res. Ther. 4(4):12912; 2013.
28. Tambuyzer, B. R.; Bergwerf, I.; De Vocht, N.; Reekmans, K.; Daans, J.; Jorens, P. G.; Goossens, H.; Ysebaert, D. K.; Chatterjee, S.; Van Marck, E.; Berneman, Z. N.; Ponsaerts, P. Allogeneic stromal cell implantation in brain tissue leads to robust microglial activation. Immunol. Cell Biol. 87(4): 267-273; 2009.
29. Yu, S.; Tajiri, N.; Franzese, N.; Franzblau, M.; Bae, E.; Platt, S.; Kaneko, Y.; Borlongan, C. V. Stem cell-like dog placenta cells afford neuroprotection against ischemic stroke model via heat shock protein upregulation. PLoS One 8(9):e76329; 2013.
30. Zeger, S. L.; Liang, K. Y.; Albert, P. S. Models for longitudinal data-A generalized estimating equation approach. Biometrics 44(4):1049-1060; 1988.