- About this Journal
- Abstracting and Indexing
- Aims and Scope
- Article Processing Charges
- Articles in Press
- Author Guidelines
- Bibliographic Information
- Citations to this Journal
- Contact Information
- Editorial Board
- Editorial Workflow
- Free eTOC Alerts
- Publication Ethics
- Reviewers Acknowledgment
- Submit a Manuscript
- Subscription Information
- Table of Contents
Journal of Allergy
Volume 2012 (2012), Article ID 187408, 8 pages
Immunomodulatory Effects of Mesenchymal Stromal Cells in Crohn’s Disease
1Department of Gastroenterology and Hepatology, Leiden University Medical Center, 2333 ZA Leiden, The Netherlands
2Division of Digestive Diseases, University of California Los Angeles, Los Angeles, CA 90095, USA
Received 21 May 2012; Accepted 27 August 2012
Academic Editor: Valentina Di Felice
Copyright © 2012 Ilse Molendijk et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- E. V. Loftus Jr. and W. J. Sandborn, “Epidemiology of inflammatory bowel disease,” Gastroenterology Clinics of North America, vol. 31, no. 1, pp. 1–20, 2002.
- C. Abraham and J. H. Cho, “Inflammatory bowel disease,” The New England Journal of Medicine, vol. 361, no. 21, pp. 2066–2078, 2009.
- G. Van Assche, A. Dignass, J. Panes et al., “The second European evidence-based consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis,” Journal of Crohn's and Colitis, vol. 4, no. 1, pp. 7–27, 2010.
- I. Logan and C. L. Bowlus, “The geoepidemiology of autoimmune intestinal diseases,” Autoimmunity Reviews, vol. 9, no. 5, pp. A372–A378, 2010.
- D. Subasinghe, N. M. M. Nawarathna, and D. N. Samarasekera, “Disease characteristics of inflammatory bowel disease (IBD): findings from a tertiary care centre in South Asia,” Journal of Gastrointestinal Surgery, vol. 15, pp. 1562–1567, 2011.
- D. C. Baumgart and W. J. Sandborn, “Inflammatory bowel disease: clinical aspects and established and evolving therapies,” The Lancet, vol. 369, no. 9573, pp. 1641–1657, 2007.
- D. A. Schwartz, E. V. Loftus Jr., W. J. Tremaine et al., “The natural history of fistulizing Crohn's disease in Olmsted County, Minnesota,” Gastroenterology, vol. 122, no. 4, pp. 875–880, 2002.
- M. A. Kamm and S. C. Ng, “Perianal fistulizing Crohn's disease: a call to action,” Clinical Gastroenterology and Hepatology, vol. 6, no. 1, pp. 7–10, 2008.
- R. T. Lewis and D. J. Maron, “Efficacy and complications of surgery for Crohn's disease,” Gastroenterology and Hepatology, vol. 6, no. 9, pp. 587–596, 2010.
- B. Bressler and B. E. Sands, “Review article: medical therapy for fistulizing Crohn's disease,” Alimentary Pharmacology and Therapeutics, vol. 24, no. 9, pp. 1283–1293, 2006.
- P. J. van Koperen, F. Safiruddin, W. A. Bemelman, and J. F. M. Slors, “Outcome of surgical treatment for fistula in ano in Crohn's disease,” British Journal of Surgery, vol. 96, no. 6, pp. 675–679, 2009.
- J. C. Hoffmann, N. N. Pawlowski, A. A. Kühl, W. Höhne, and M. Zeitz, “Animal models of inflammatory bowel disease: an overview,” Pathobiology, vol. 70, no. 3, pp. 121–130, 2003.
- S. Wirtz, C. Neufert, B. Weigmann, and M. F. Neurath, “Chemically induced mouse models of intestinal inflammation,” Nature Protocols, vol. 2, no. 3, pp. 541–546, 2007.
- A. A. te Velde, M. I. Verstege, and D. W. Hommes, “Critical appraisal of the current practice in murine TNBS-induced colitis,” Inflammatory Bowel Diseases, vol. 12, no. 10, pp. 995–999, 2006.
- E. M. Horwitz, K. Le Blanc, M. Dominici et al., “Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 7, no. 5, pp. 393–395, 2005.
- A. I. Caplan, “The mesengenic process,” Clinics in Plastic Surgery, vol. 21, no. 3, pp. 429–435, 1994.
- M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999.
- K. Le Blanc, C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringdén, “HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells,” Experimental Hematology, vol. 31, no. 10, pp. 890–896, 2003.
- P. A. Zuk, M. Zhu, P. Ashjian et al., “Human adipose tissue is a source of multipotent stem cells,” Molecular Biology of the Cell, vol. 13, no. 12, pp. 4279–4295, 2002.
- T. Tondreau, N. Meuleman, A. Delforge et al., “Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity,” Stem Cells, vol. 23, no. 8, pp. 1105–1112, 2005.
- A. Erices, P. Conget, and J. J. Minguell, “Mesenchymal progenitor cells in human umbilical cord blood,” British Journal of Haematology, vol. 109, no. 1, pp. 235–242, 2000.
- P. S. In't Anker, S. A. Scherjon, C. Kleijburg-van der Keur et al., “Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta,” Stem Cells, vol. 22, no. 7, pp. 1338–1345, 2004.
- Q. Zhang, S. Shi, Y. Liu et al., “Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis,” Journal of Immunology, vol. 183, no. 12, pp. 7787–7798, 2009.
- M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006.
- D. G. Phinney and D. J. Prockop, “Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views,” Stem Cells, vol. 25, no. 11, pp. 2896–2902, 2007.
- M. D. Nicola, C. Carlo-Stella, M. Magni et al., “Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli,” Blood, vol. 99, no. 10, pp. 3838–3843, 2002.
- M. Krampera, S. Glennie, J. Dyson et al., “Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide,” Blood, vol. 101, no. 9, pp. 3722–3729, 2003.
- J. A. Potian, H. Aviv, N. M. Ponzio, J. S. Harrison, and P. Rameshwar, “Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens,” Journal of Immunology, vol. 171, no. 7, pp. 3426–3434, 2003.
- W. T. Tse, J. D. Pendleton, W. M. Beyer, M. C. Egalka, and E. C. Guinan, “Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation,” Transplantation, vol. 75, no. 3, pp. 389–397, 2003.
- A. J. Nauta, G. Westerhuis, A. B. Kruisselbrink, E. G. A. Lurvink, R. Willemze, and W. E. Fibbe, “Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting,” Blood, vol. 108, no. 6, pp. 2114–2120, 2006.
- S. Aggarwal and M. F. Pittenger, “Human mesenchymal stem cells modulate allogeneic immune cell responses,” Blood, vol. 105, no. 4, pp. 1815–1822, 2005.
- X. X. Jiang, Y. Zhang, B. Liu et al., “Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells,” Blood, vol. 105, no. 10, pp. 4120–4126, 2005.
- S. Beyth, Z. Borovsky, D. Mevorach et al., “Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness,” Blood, vol. 105, no. 5, pp. 2214–2219, 2005.
- G. M. Spaggiari, H. Abdelrazik, F. Becchetti, and L. Moretta, “MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2,” Blood, vol. 113, no. 26, pp. 6576–6583, 2009.
- S. Glennie, I. Soeiro, P. J. Dyson, E. W. F. Lam, and F. Dazzi, “Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells,” Blood, vol. 105, no. 7, pp. 2821–2827, 2005.
- E. Zappia, S. Casazza, E. Pedemonte et al., “Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy,” Blood, vol. 106, no. 5, pp. 1755–1761, 2005.
- T. Takahashi, Y. Kuniyasu, M. Toda et al., “Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state,” International Immunology, vol. 10, no. 12, pp. 1969–1980, 1998.
- R. Maccario, M. Podestà, A. Moretta et al., “Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4 + T-cell subsets expressing a regulatory/suppressive phenotype,” Haematologica, vol. 90, no. 4, pp. 516–525, 2005.
- D. M. Sansom and L. S. K. Walker, “The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology,” Immunological Reviews, vol. 212, pp. 131–148, 2006.
- M. A. González, E. Gonzalez-Rey, L. Rico, D. Büscher, and M. Delgado, “Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses,” Gastroenterology, vol. 136, no. 3, pp. 978–989, 2009.
- E. Gonzalez-Rey, P. Anderson, M. A. González, L. Rico, D. Büscher, and M. Delgado, “Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis,” Gut, vol. 58, no. 7, pp. 929–939, 2009.
- B. Parekkadan, R. Upadhyay, J. Dunham et al., “Bone marrow stromal cell transplants prevent experimental enterocolitis and require host CD11b+ splenocytes,” Gastroenterology, vol. 140, no. 3, pp. 966–975, 2011.
- S. Ghannam, J. Pène, G. Torcy-Moquet, C. Jorgensen, and H. Yssel, “Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype,” Journal of Immunology, vol. 185, no. 1, pp. 302–312, 2010.
- L. Liang, C. Dong, X. Chen, et al., “Human umbilical cord mesenchymal stem cells ameliorate mice trinitrobenzene sulfonic acid (TNBS)-induced colitis,” Cell Transplantation, vol. 20, pp. 1395–1408, 2011.
- G. M. Spaggiari, A. Capobianco, S. Becchetti, M. C. Mingari, and L. Moretta, “Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation,” Blood, vol. 107, no. 4, pp. 1484–1490, 2006.
- R. D. Newberry, J. S. McDonough, W. F. Stenson, and R. G. Lorenz, “Spontaneous and continuous cyclooxygenase-2-dependent prostaglandin E2 production by stromal cells in the murine small intestine lamina propria: directing the tone of the intestinal immune response,” Journal of Immunology, vol. 166, no. 7, pp. 4465–4472, 2001.
- M. M. Duffy, J. Pindjakova, S. A. Hanley, et al., “Mesenchymal stem cell inhibition of T-helper 17 cell-differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor,” European Journal of Immunology, vol. 41, pp. 2840–2851, 2011.
- C. Bouffi, C. Bony, G. Courties, C. Jorgensen, and D. Noël, “IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis,” PLoS ONE, vol. 5, no. 12, Article ID e14247, 2010.
- F. Tanaka, K. Tominaga, M. Ochi et al., “Exogenous administration of mesenchymal stem cells ameliorates dextran sulfate sodium-induced colitis via anti-inflammatory action in damaged tissue in rats,” Life Sciences, vol. 83, no. 23-24, pp. 771–779, 2008.
- G. Ren, L. Zhang, X. Zhao et al., “Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide,” Cell Stem Cell, vol. 2, no. 2, pp. 141–150, 2008.
- M. Zwolinska-Wcislo, T. Brzozowski, A. Ptak-Belowska et al., “Nitric oxide-releasing aspirin but not conventional aspirin improves healing of experimental colitis,” World Journal of Gastroenterology, vol. 17, pp. 4076–4089, 2011.
- G. Ren, J. Su, L. Zhang et al., “Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression,” Stem Cells, vol. 27, no. 8, pp. 1954–1962, 2009.
- G. M. Spaggiari, A. Capobianco, H. Abdelrazik, F. Becchetti, M. C. Mingari, and L. Moretta, “Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2,” Blood, vol. 111, no. 3, pp. 1327–1333, 2008.
- M. Krampera, L. Cosmi, R. Angeli et al., “Role for interferon-γ in the immunomodulatory activity of human bone marrow mesenchymal stem cells,” Stem Cells, vol. 24, no. 2, pp. 386–398, 2006.
- M. Duijvestein, M. E. Wildenberg, M. M. Welling, et al., “Pretreatment with interferon-γ enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis,” Stem Cells, vol. 29, pp. 1549–1558, 2011.
- M. Duijvestein, A. C. W. Vos, H. Roelofs et al., “Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study,” Gut, vol. 59, no. 12, pp. 1662–1669, 2010.
- D. García-Olmo, M. García-Arranz, D. Herreros, I. Pascual, C. Peiro, and J. A. Rodríguez-Montes, “A phase I clinical trial of the treatment of crohn's fistula by adipose mesenchymal stem cell transplantation,” Diseases of the Colon and Rectum, vol. 48, no. 7, pp. 1416–1423, 2005.
- D. Garcia-Olmo, D. Herreros, I. Pascual et al., “Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase ii clinical trial,” Diseases of the Colon and Rectum, vol. 52, no. 1, pp. 79–86, 2009.
- R. Ciccocioppo, M. E. Bernardo, A. Sgarella et al., “Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease,” Gut, vol. 60, no. 6, pp. 788–798, 2011.
- M. Duijvestein, I. Molendijk, H. Roelofs, et al., “Mesenchymal stromal cell function is not affected by drugs used in the treatment of inflammatory bowel disease,” Cytotherapy, vol. 13, pp. 1066–1073, 2011.
- M. Allison, “Genzyme backs osiris, despite prochymal flop,” Nature Biotechnology, vol. 27, no. 11, pp. 966–967, 2009.
- M. François, I. B. Copland, S. Yuan, R. Romieu-Mourez, E. K. Waller, and J. Galipeau, “Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-γ licensing,” Cytotherapy, vol. 14, pp. 147–152, 2012.
- A. I. Caplan, “Adult mesenchymal stem cells for tissue engineering versus regenerative medicine,” Journal of Cellular Physiology, vol. 213, no. 2, pp. 341–347, 2007.
- A. Stolzing, E. Jones, D. McGonagle, and A. Scutt, “Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies,” Mechanisms of Ageing and Development, vol. 129, no. 3, pp. 163–173, 2008.
- M. Zaim, S. Karaman, G. Cetin, and S. Isik, “Donor age and long-term culture affect differentiation and proliferation of human bone marrow mesenchymal stem cells,” Annals of Hematology, vol. 91, pp. 1175–1186, 2012.
- W. Li, G. Ren, Y. Huang, et al., “Mesenchymal stem cells: a double-edged sword in regulating immune responses,” Cell Death & Differentiation, vol. 19, pp. 1505–1513, 2012.