Temporal HLA profiling and immunomodulatory effects of human adult bone marrow- and adipose-derived mesenchymal stem cells

Regenerative Medicine

Volumn 9, Issue 1, 2014, Pages 67-79

  Purandare, Bhamini ^a   Teklemariam, Takele ^a   Zhao, Longmei ^a   Hantash, Basil M ^a  

^a Escape Therapeutics Inc   (United States)

Author keywords

cytotoxicity; HLA; immunomodulation; mesenchymal stem cells; temporal expression

Indexed keywords

HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; MESSENGER RNA;

ADIPOSE DERIVED STEM CELL; ADULT STEM CELL; ANTIGEN EXPRESSION; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; MESENCHYMAL STEM CELL; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; STEM CELL EXPANSION;

ADIPOSE TISSUE; ADULT; ADULT STEM CELLS; BLOTTING, WESTERN; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION PROFILING; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNOLOGIC FACTORS; MESENCHYMAL STROMAL CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84891074881     PISSN: 17460751     EISSN: 1746076X     Source Type: Journal    
DOI: 10.2217/rme.13.82     Document Type: Article

References (41)

1. Pittenger MF, Mackay AM, Beck SC et al. Multilineage potential of adult human mesenchymal stem cells. Science 284(5411), 143-147 (1999). Characterized adult mesenchymal stem cells (MSCs) and revealed that MSCs have the capacity to proliferate and differentiate into multiple lineages, such as osteogenic, chondrogenic and adipogenic cells in vitro (Pubitemid 29282067)
2. Characterized adult mesenchymal stem cells (MSCs) and revealed that MSCs have the capacity to proliferate and differentiate into multiple lineages, such as osteogenic, chondrogenic and adipogenic cells in vitro. 2 Zuk PA, Zhu M, Ashjian P et al. Human adipose tissue is a source of multi-potent stem cells. Mol. Biol. Cell 13(12), 4279-4295 (2002) (Pubitemid 35471185)
3. Zuk PA, Zhu M, Mizuno H et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7(2), 211-228 (2001) (Pubitemid 32295155)
4. Divya MS, Roshin GE, Divya TS et al. Umbilical cord blood-derived mesenchymal stem cells consist of a unique population of progenitors co-expressing mesenchymal stem cell and neuronal markers capable of instantaneous neuronal differentiation. Stem Cell Res. Ther. 3(6), 57 (2012)
5. Belicchi M, Pisati F, Lopa Ret al. Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J. Neurosci. Res. 77(4), 475-486 (2004) (Pubitemid 39006999)
6. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenasemediated tryptophan degradation. Blood 103(12), 4619-4621 (2004) (Pubitemid 38745993)
7. Di Nicola M, Carlo-Stella C, Magni M et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99(10), 3838-3843 (2002). Demonstrates that in vitro-expanded bonemarrow MSCs suppress T-cell proliferation triggered by allogeneic peripheral blood mononuclear cells or nonspecific mitogens, such as phytohemagglutinin. (Pubitemid 34534559)
8. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L. 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 107(4), 1484-1490 (2006). nn Describes the interaction of MSCs with natural killer cells and provides evidence that IL-2-Activated natural killer cells lyze both autologous and allogeneic MSCs. (Pubitemid 43242385)
9. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J. Immunol. 177(4), 2080-2087 (2006) (Pubitemid 44200965)
10. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4), 1815-1822 (2005). n Describes the interaction of MSCs with different immune cells and provides mechanisms of MSC-mediated immunomodulation. (Pubitemid 40223708)
11. Ren G, Zhang L, Zhao X et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2(2), 141-150 (2008) (Pubitemid 351181031)
12. Selmani Z, Naji A, Gaiffe E et al. HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation 87(Suppl. 9), S62-S66 (2009)
13. Ayala Garcia MA, Gonzalez Yebra B, Lopez Flores AL, Guani Guerra E. The major histocompatibility complex in transplantation. J. Transplant. 2012, 842141 (2012)
14. Morishima Y, Sasazuki T, Inoko H et al. The clinical significance of human leukocyte antigen (HLA) allele compatibility in patients receiving a marrow transplant from serologically HLA-A, HLA-B, and HLA-DR matched unrelated donors. Blood 99(11), 4200-4206 (2002) (Pubitemid 35332066)
15. Petersdorf EW, Kollman C, Hurley CK et al. Effect of HLA class II gene disparity on clinical outcome in unrelated donor hematopoietic cell transplantation for chronic myeloid leukemia: the US national marrow donor program experience. Blood 98(10), 2922-2929 (2001)
16. 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. 31(10), 890-896 (2003) (Pubitemid 37211373)
17. Le Blanc K. Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy 5(6), 485-489 (2003) (Pubitemid 38028708)
18. Nasef A, Mathieu N, Chapel A et al. Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G. Transplantation 84(2), 231-237 (2007) (Pubitemid 47205757)
19. Herrmann R, Sturm M, Shaw K et al. Mesenchymal stromal cell therapy for steroidrefractory acute and chronic graft versus host disease: a Phase 1 study. Int. J. Hematol. 95(2), 182-188 (2012)
20. Connick P, Kolappan M, Crawley C et al. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label Phase 2a proof-ofconcept study. Lancet Neurol. 11(2), 150-156 (2012)
21. Karamouzian S, Nematollahi-Mahani SN, Nakhaee N, Eskandary H. Clinical safety and primary efficacy of bone marrow mesenchymal cell transplantation in subacute spinal cord injured patients. Clin. Neurol. Neurosurg. 114(7), 935-939 (2012)
22. Macmillan ML, Blazar BR, Defor TE, Wagner JE. Transplantation of ex-vivo culture-expanded parental haploidentical mesenchymal stem cells to promote engraftment in pediatric recipients of unrelated donor umbilical cord blood: results of a Phase III clinical trial. Bone Marrow Transplant. 43(6), 447-454 (2009)
23. Jones EA, Kinsey SE, English A et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 46(12), 3349-3360 (2002) (Pubitemid 35453547)
24. Zhao L, Abdollah P, Do S, Nye C, Hantash BM. Novel negative selection marker CD54 enhances differentiation of human adiposederived mesenchymal stem cells. J. Clin. Cell Immunol. S9, 005 (2013)
25. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multi-potent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8(4), 315-317 (2006) (Pubitemid 44269669)
26. Zhao L, Purandare B, Zhang J, Hantash BM. Beta 2-microglobulin-free HLA-G activates natural killer cells by increasing cytotoxicity and proinflammatory cytokine production. Hum. Immunol. 74(4), 417-424 (2012)
27. Riteau B, Rouas-Freiss N, Menier C, Paul P, Dausset J, Carosella ED. HLA-G2, -G3, and -G4 isoforms expressed as non-mature cell surface glycoproteins inhibit NK and antigenspecific CTL cytolysis. J. Immunol. 166(8), 5018-5026 (2001) (Pubitemid 32280714)
28. Rizzo R, Lanzoni G, Stignani M et al. A simple method for identifying bone marrow mesenchymal stromal cells with a high immunosuppressive potential. Cytotherapy 13(5), 523-527 (2011)
29. Nauta AJ, Westerhuis G, Kruisselbrink AB, Lurvink EG, Willemze R, Fibbe WE. Donorderived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood 108(6), 2114-2120 (2006). Examines the immunosuppressive properties of MSCs in vivo in an allogeneic transplantation model. The results demonstrate that allogeneic MSCs are not intrinsically immunoprivileged and may induce immune responses, resulting in rejection of the allogeneic MSC graft. (Pubitemid 44395028)
30. Natarajan K, Li H, Mariuzza RA, Margulies DH. MHC class I molecules, structure and function. Rev. Immunogenet. 1(1), 32-46 (1999)
31. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet 373(9674), 1550-1561 (2009)
32. 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. 57(1), 11-20 (2003) (Pubitemid 38019084)
33. O'Callaghan CA, Bell JI. Structure and function of the human MHC class Ib molecules HLA-E, HLA-F and HLA-G. Immunol. Rev. 163, 129-138 (1998) (Pubitemid 28327866)
34. Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cellmediated lysis. J. Exp. Med. 187(5), 813-818 (1998) (Pubitemid 28115198)
35. Weiss EH, Lilienfeld BG, Muller S et al. HLA-E/human beta 2-microglobulin transgenic pigs: protection against xenogeneic human anti-pig natural killer cell cytotoxicity. Transplantation 87(1), 35-43 (2009)
36. Gotherstrom C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K. Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica 90(8), 1017-1026 (2005) (Pubitemid 41323500)
37. Ivanova-Todorova E, Mourdjeva M, Kyurkchiev D et al. HLA-G expression is up-regulated by progesterone in mesenchymal stem cells. Am. J. Reprod. Immunol. 62(1), 25-33 (2009)
38. Sotiropoulou PA, Perez SA, Salagianni M, Baxevanis CN, Papamichail M. Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells. Stem Cells 24(2), 462-471 (2006) (Pubitemid 44464816)
39. Potian JA, Aviv H, Ponzio NM, Harrison JS, Rameshwar P. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J. Immunol. 171(7), 3426-3434 (2003) (Pubitemid 37254543)
40. Delarosa O, Lombardo E, Beraza A et al. Requirement of IFN-gamma-mediated indoleamine 2,3-dioxygenase expression in the modulation of lymphocyte proliferation by human adipose-derived stem cells. Tissue Eng. Part A 15(10), 2795-2806 (2009)
41. Melief SM, Zwaginga JJ, Fibbe WE, Roelofs H. Adipose tissue-derived multipotent stromal cells have a higher immunomodulatory capacity than their bone marrow-derived counterparts. Stem Cells Transl. Med. 2(6), 455-463 (2013). Adipose-derived MSCs appear to possess a superior immunosuppressive capacity to bone marrow-derived MSCs, and can be used as a good alternative to bone marrowderived MSCs for immunomodulatory therapy.