Why are MSCs therapeutic? New data: New insight

Journal of Pathology

Volumn 217, Issue 2, 2009, Pages 318-324

  Caplan, A I ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone marrow; CFU F; Mesenchymal stem cell; Therapeutics

Indexed keywords

COLONY STIMULATING FACTOR 1; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 11; INTERLEUKIN 3; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR; STEM CELL FACTOR; TRANSFORMING GROWTH FACTOR BETA2;

ADULT STEM CELL; ANGIOGENESIS; APOPTOSIS; ASTHMA; AUTOIMMUNITY; BONE MARROW; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CLINICAL TRIAL; CROHN DISEASE; FIBROBLAST; HEART ARRHYTHMIA; HEART VENTRICLE EXTRASYSTOLE; HUMAN; IMMUNOMODULATION; ISCHEMIA; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NEUROLOGIC DISEASE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; TISSUE INJURY;

ADULT; ADULT STEM CELLS; AUTOIMMUNITY; HUMANS; IMMUNE SYSTEM; MESENCHYMAL STEM CELLS; PERICYTES; STEM CELL NICHE; STEM CELL TRANSPLANTATION;

EID: 58449135981     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2469     Document Type: Review

References (60)

1. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007;213:341-347.
2. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991;9:641-650.
3. Caplan AI. Mesenchymal stem cell: cell-based reconstructive therapy in orthopaedics. Tiss Eng 2005;11:1198-1211.
4. Thomas Ed, Blume KG. Historical markers in the development of allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transpl 1999;5:341-346.
5. Weiss L. The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats. Anat Rec 1976;186:161-184.
6. Bruder SP and Caplan AI. Osteogenic cell lineage analysis is facilitated by organ culture of embryonic chick periosteum. Dev Biol 1990;141:319-329.
7. Caplan AI and Boyan BD. Endochondral bone formation: the lineage cascade. In Bone, vol 8, Hall B (ed.). CRC Press: Boca Raton, FL, 1994; 1-46.
8. Haynesworth SE, Goldberg VM, Caplan AI. Diminution of the number of mesenchymal stem cells as a cause for skeletal aging. In Musculoskeletal Soft-tissue Aging: Impact on Mobility, section 1, Buckwalter JA, Goldberg VM, Y Woo SL-Y (eds). American Academy of Orthopaedic Surgeons: Rosemont, IL, USA, 1994; 79-87.
9. Lennon DP, Haynesworth SE, Bruder SP, Jaiswall N, Caplan AI. Human and animal mesenchymal progenitor cells from bone marrow: identification of serum for optimal selection and proliferation. In vitro Cell Dev Biol 1996;32:602-611.
10. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968;6:230-247.
11. Owen M, Friedenstein AJ. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 1988;136:42-60.
12. Caplan AI. Stem cell delivery vehicle. Biomaterials 1990;11:44-46.
13. Ohgushi H, Goldberg VM and Caplan AI. Heterotopic osteogenesis in porous ceramics induced by marrow cells. J Orthop Res 1989;7:568-578.
14. Goshima J, Goldberg VM, Caplan AI. The origin of bone formed in composite grafts of porous calcium phosphate ceramic loaded with marrow cells. Clin Orthop Rel Res 1991;269:274-283.
15. Allay JA, Dennis JE, Haynesworth SE, Majumdar M, Clapp DW, Caplan AI, et al. LacZ and IL-3 expression in vivo after retroviral transduction of marrow-derived human osteogenic mesenchymal progenitors. Human Gene Therapy 1997;8:1417-1427.
16. Dennis JE, Caplan AI. Porous ceramic vehicles for rat-marrow-derived (Rattus norvegicus) osteogenic cell delivery: effects of pre-treatment with fibronectin or laminin. J Oral Implant 1993;19:106-115.
17. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003;57:11-20.
18. Maitra B, Szekely E, Gjini K, Laughlin MJ, Dennis J, Haynesworth SE, et al. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T cell activation Bone Marrow Transpl 2004;33:597-604.
19. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003;31:890.
20. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003;75:389.
21. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003;101:3722.
22. Lazarus HM, Haynesworth SE, Gerson SL, Rosenthal N, Caplan AI. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells; MPCs): implications for therapeutic use. Bone Marrow Transpl 1995;16:557-564.
23. Koc ON, Peters C, Aubourg P, Raghavan S, Dyhouse S, DeGasperi R, et al. Bone marrow derived mesenchymal stem cells remain host-derived despite successful hematopoietic engraftment after allogeneic transplantation in patients with lysosomal and peroxisomal storage diseases. Exp Hemtaol 1999;27:1675-1681.
24. Koc ON, Gerson SL, Cooper BW, Dyhouse SM, Haynesworth SE, Caplan AI, et al. Rapid hematopoietic recovery after co-infusion of autologous blood stem cells and culture expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high dose chemotherapy. J Clin Oncol 2000;18:307-316.
25. Koc ON, Day J, Nieder M, Gerson SL, Lazarus HM, Krivit W. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transpl 2002;30:215-22.
26. Devine SM, Bartholomew AM, Mahmud N, Nelson M, Patil S, Hardy W, et al. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol 2001;29:244- 255.
27. Majumdar MK, Thiede MA, Mosca JD, Moorman M, Gerson SL. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. JCell Physiol 1998;176:57-66.
28. Haynesworth SE, Baber MA, Caplan AI. Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1α. J Cell Physiol 1996;166:585-592.
29. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WWK, Gordon PL, Neel, M, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309-313.
30. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, et al. Isolated allogeneic bone marrow-derived mes- enchymal cells engraft and stimulate growth in children with osteo- genesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci USA 2002;99:8932-8937.
31. PittengerMD, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
32. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008;371: 1579-1586.
33. Gao J, Dennis JE, Muzic RF, Lundberg M and Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 2001;169:12-20.
34. Mangi AA, Noiseux N, Kong D, He H, Rezvani M, Ingwall JS, et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003;10:10.
35. Taylor DA, Atkins BZ, Hungspreugs P, Jones TR, Reedy MC, Hutcheson KA, et al. Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nat Med 1998;4:929-933.
36. Murry CE, Wiseman RW, Schwartz SM, Hauschka SD. Skeletal myoblast transplantation for repair of myocardial necrosis. J Clin Invest 1996;98:2512-2523.
37. Saito T, Dennis JE, Lennon DP, Young RG, Caplan AI. Myogenic expression of mesenchymal stem cells within myotubes of MDX mice in vitro and in vivo. Tissue Eng 1996;1:327-344.
38. Wakitani S, Saito T, Caplan AI. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 1995;18:1417-1426.
39. Caparrelli DJ, Cattaneo SM, Shake JG, Flynn EC, Meyers J, Baumgartner WA, et al. Cellular myoplasty with mesenchymal stem cells results in improved cardiac performance in a swine model of myocardial infarction. Circulation 2001;104:II-599 (Abstr).
40. Askari A, Unzek S, Popovic ZB, et al. Effect of stromal-cell-derived factor-1 on stem cell homing and tissue regeneration in ischemic cardiomyopathy. Lancet 2003;362:697-703.
41. Schenk S, Mal N, Finan A, Zhang M, Kiedrowski M, Popovic Z, et al. Monocyte chemotactic protein-3 is a myocardial mesenchy-mal stem cell homing factor. Stem Cells 2007;25:245-251.
42. Murphy J, Fink D, Hunsiker E, Barry F. Stem cell therapy in a caprine model of osteoarthritis. Arthrit Rheum 2003;48:3464-3474.
43. Li Y, Chen J, Chen XG Wang L, Gautam SC, Zu YX, et al. Human marrow stromal cell therapy for stroke in rat: neurotrophic and functional recovery. Neurology 2002;59:514-523.
44. Mahmood A, Lu D, Lu M, Chopp M. Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 2003;53:697-703.
45. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076-1084.
46. Singer M. The trophic quality of the neuron: some theoretical considerations. Prog Brain Res 1964;13:228-232.
47. Fleming, Jr. JE, Cassiede P, Baber M, Haynesworth SE, Caplan AI. A Monoclonal antibody against adult marrow-derived mesenchy-mal cells recognizes developing vasculature in embryonic human skin. Dev Dyn 1998;212:119-132.
48. Sorrell JM, Baber MA, Caplan AI. A self-assembled fibrob- last-endothelial cell co-culture system that supports in vitro vas-culogenesis by both human umbilical vein endothelial cells and human dermal microvascular endothelial cells. Cells Tissues Organs 2007;186:157-168.
49. Sorrell JM, Baber MA, Caplan AI. Influence of adult mesenchymal stem cells on in vitro vascular formation. TissEng A 2008;(in press).
50. Crisan M, Deasy B, Favina M, Zheng B, Huard J, Lazzari L, et al. Purification and long-term culture of multipotent progenitor cells affiliated with the walls of human blood vessels: myoendothe- lial cells and pericytes. Methods Cell Biol 2008;86:295-309.
51. Sacchetti B, Funari A, Michienzi S, DiCesare S, Piersanti S, Saggio I, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007;131:324-336.
52. Brighton CT, Lorich DG, Kupcha R, Reilly TM, Jones AR, Woodbury RA. The pericyte as a possible osteoblast progenitor cell. Clin Orthop Relat Res 1992;275:287-99.
53. AI Caplan. All MSCs are pericytes? Cell Stem Cell 2008;3(3):229-230.
54. da Silva Meirelles L, Caplan AI, Nardi NB. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008;26:2287-2299.
55. Sinsicalco D, Sullo N, Maione S, Rossi F, D'Agostino B. Review. Stem cell therapy: the great promise in lung disease. Therap Adv Resp Dis 2008;2:173-177.
56. Chen MF, Lin CT, Chen WC, Yang CT, Chen CC, Lia SK, et al. The sensitivity of human mesenchymal stem cells to ionizing radiation. Int J Radiat Oncol Biol Phys 2006;66(1): 244- 253.
57. Bai L, Caplan AI, Lennon DL, Miller RH. Human mesenchymal stem cell signals regulate neural stem cell fate. Neurochem Res 2007;32:353-362.
58. Dennis JE, Cohen N, Goldberg VM, Caplan AI. Targeted delivery of progenitor cells for cartilage repair. J Orthop Res 2004;22:735- 741.
59. Estes BT, Wu AW, Guilak F. Potent induction of chon-drocytic differential of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthrit Rheum 2006; 54(4):1222-1232.
60. da Silva Meirelles L, Sand TT, Harman RJ, Lennon DP, Caplan AI. MSC frequency correlates with blood vessel density in equine adipose tissue. Tiss Eng A 2008;14:(in press).