Intradermal injections of equine allogeneic umbilical cord-derived mesenchymal stem cells are well tolerated and do not elicit immediate or delayed hypersensitivity reactions

Cytotherapy

Volumn 13, Issue 10, 2011, Pages 1180-1192

  Carrade, Danielle D ^a   Affolter, Verena K ^a   Outerbridge, Catherine A ^a   Watson, Johanna L ^a   Galuppo, Larry D ^a   Buerchler, Sabine ^a   Kumar, Vijay ^b   Walker, Naomi J ^a   Borjesson, Dori L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Thermogenesis Corp   (United States)

Author keywords

equine; immune response; intradermal injection; mesenchymal stem cells; umbilical cord tissue

Indexed keywords

ACUTE GRAFT REJECTION; ALLOGENEIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGENICITY; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CELL STRUCTURE; CELL THERAPY; CELLULAR IMMUNITY; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; CORD BLOOD STEM CELL TRANSPLANTATION; DELAYED HYPERSENSITIVITY; DERMATITIS; DRUG SAFETY; HISTOPATHOLOGY; HORSE; HUMAN; HUMAN CELL; IMMEDIATE TYPE HYPERSENSITIVITY; IN VITRO STUDY; INJECTION SITE EDEMA; INJECTION SITE INDURATION; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL; MIXED LYMPHOCYTE REACTION; NONHUMAN; PRIORITY JOURNAL; RETICULOENDOTHELIOSIS; SKIN EDEMA; T LYMPHOCYTE; URTICARIA;

EID: 80054767704     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.3109/14653249.2011.602338     Document Type: Article

References (51)

1. Arnhold SJ, Goletz I, Klein H, Stumpf G, Beluche LA, Rohde C, et al. Isolation and characterization of bone marrowderived equine mesenchymal stem cells. Am J Vet Res. 2007; 68:1095-105. (Pubitemid 47616621)
2. Fortier LA, Nixon AJ, Williams J, Cable CS. Isolation and chondrocytic differentiation of equine bone marrow-derived mesenchymal stem cells. Am J Vet Res. 1998;59:1182-7. (Pubitemid 128472445)
3. Toupadakis CA, Wong A, Genetos DC, Cheung WK, Borjesson DL, Ferraro GL, et al. Comparison of the osteogenic potential of equine mesenchymal stem cells from bone marrow, adipose tissue, umbilical cord blood, and umbilical cord tissue. Am J Vet Res.71:1237-45.
4. Vidal MA, Kilroy GE, Johnson JR, Lopez MJ, Moore RM, Gimble JM. Cell growth characteristics and differentiation frequency of adherent equine bone marrow-derived mesenchymal stem cells: Adipogenic and osteogenic capacity. Vet Surg. 2006;35:601-10. (Pubitemid 44526659)
5. Vidal MA, Kilroy GE, Lopez MJ, Johnson JR, Moore RM, Gimble JM. Characterization of equine adipose tissue-derived stem cells: Adipogenic and osteogenic capacity and comparison with bone marrow-derived mesenchymal stem cells. Vet Surg. 2007;36:613-22. (Pubitemid 47480926)
6. Carrade DD, Owens SD, Galuppo LD, Vidal MA, Ferraro GL, Librach F, et al. Clinicopathologic fi ndings following intra-articular injection of autologous and allogeneic placentally derived equine mesenchymal stem cells in horses. Cytotherapy. 2011;13:419-30.
7. Passeri S, Nocchi F, Lamanna R, Lapi S, Miragliotta V, Giannessi E, et al. Isolation and expansion of equine umbilical cordderived matrix cells (EUCMCs). Cell Biol Int. 2009;33:100-5.
8. Koch TG, Heerkens T, Thomsen PD, Betts DH. Isolation of mesenchymal stem cells from equine umbilical cord blood. BMC Biotechnol. 2007;7:26.
9. Koch TG, Thomsen PD, Betts DH. Improved isolation protocol for equine cord blood-derived mesenchymal stem cells. Cytotherapy. 2009;11:443-7.
10. Schuh EM, Friedman MS, Carrade DD, Li J, Heeke D, Oyserman SM, et al. Identifi cation of variables that optimize isolation and culture of multipotent mesenchymal stem cells from equine umbilical-cord blood. Am J Vet Res. 2009;70:1526-35.
11. Conconi MT, Burra P, Di Liddo R, Calore C, Turetta M, Bellini S, et al. CD105(+) cells from Wharton ' s jelly show in vitro and in vivo myogenic differentiative potential. Int J Mol Med. 2006;18:1089-96.
12. Ma L, Feng XY, Cui BL, Law F, Jiang XW, Yang LY, et al. Human umbilical cord Wharton ' s jelly-derived mesenchymal stem cell differentiation into nerve-like cells. Chin Med J (Engl). 2005;118:1987-93. (Pubitemid 47049843)
13. Mitchell KE, Weiss ML, Mitchell BM, Martin P, Davis D, Morales L, et al. Matrix cells from Wharton ' s jelly form neurons and glia. Stem Cells. 2003;21:50-60. (Pubitemid 36120365)
14. Chang CJ, Yen ML, Chen YC, Chien CC, Huang HI, Bai CH, et al. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells. 2006;24:2466-77.
15. Li C, Zhang W, Jiang X, Mao N. Human-placenta-derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cells. Cell Tissue Res. 2007;330:437-46. (Pubitemid 350098216)
16. Suzdaltseva YG, Burunova VV, Vakhrushev IV, Cheglakov IB, Yarygin KN. In vitro comparison of immunological properties of cultured human mesenchymal cells from various sources. Bull Exp Biol Med. 2008;145:228-31.
17. Weiss ML, Anderson C, Medicetty S, Seshareddy KB, Weiss RJ, VanderWerff I, et al. Immune properties of human umbilical cord Wharton ' s jelly-derived cells. Stem Cells. 2008;26: 2865-74.
18. Najar M, Raicevic G, Boufker HI, Fayyad Kazan H, De Bruyn C, Meuleman N, et al. Mesenchymal stem cells use PGE2 to modulate activation and proliferation of lymphocyte subsets: Combined comparison of adipose tissue, Wharton ' s jelly and bone marrow sources. Cell Immunol. 2010;264:171-9.
19. Kinkaid HY, Huang XP, Li RK, Weisel RD. What' s new in cardiac cell therapy? Allogeneic bone marrow stem cells as 'universal donor cells ' J Card Surg. 2010;25:359-66.
20. Tolar J, Le Blanc K, Keating A, Blazar BR. Concise review. Hitting the right spot with mesenchymal stem cells. Stem Cells. 2010;28:1446-55.
21. Prigozhina TB, Khitrin S, Elkin G, Eizik O, Morecki S, Slavin S. Mesenchymal stem cells lose their immunosuppressive potential after allotransplantation. Exp Hematol. 2008;36: 1370-6.
22. Poncelet AJ, Vercruysse J, Saliez A, Gianello P. Although pig allogeneic mesenchymal stem cells are not immunogenic in vitro, intracardiac injection elicits an immune response in vivo. Transplantation. 2007;83:783-90. (Pubitemid 46569198)
23. Arinzeh TL, Peter SJ, Archambault MP, van den Bos C, Gordon S, Kraus K, et al. Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect. J Bone Joint Surg Am. 2003;85A:1927-35. (Pubitemid 37259728)
24. Guest DJ, Smith MR, Allen WR. Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superfi cial digital fl exor tendon of horses: Preliminary study. Equine Vet J. 2008;40:178-81. (Pubitemid 351717168)
25. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA. Mesenchymal stem cells: Immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy. 2009;11:377-91.
26. Newman RE, Yoo D, LeRoux MA, Danilkovitch-Miagkova A. Treatment of infl ammatory diseases with mesenchymal stem cells. Infl amm Allergy Drug Targets. 2009;8:110-23.
27. Sotiropoulou PA, Papamichail M. Immune properties of mesenchymal stem cells. Methods Mol Biol. 2007;407:225-43.
28. Duan X, Yang L, Dong S, Xin R, Chen G, Guo L. Characterization of EGFP-labeled mesenchymal stem cells and redistribution of allogeneic cells after subcutaneous implantation. Arch Orthop Trauma Surg. 2008;128:751-9.
29. Cho PS, Messina DJ, Hirsh EL, Chi N, Goldman SN, Lo DP, et al. Immunogenicity of umbilical cord tissue derived cells. Blood. 2008;111:430-8.
30. Batten P, Sarathchandra P, Antoniw JW, Tay SS, Lowdell MW, Taylor PM, et al. Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: Relevance to tissue engineering human heart valves. Tissue Eng. 2006;12:2263-73. (Pubitemid 44734984)
31. Keyser KA, Beagles KE, Kiem HP. Comparison of mesenchymal stem cells from different tissues to suppress T-cell activation. Cell Transplant. 2007;16:555-62. (Pubitemid 351448291)
32. Prevosto C, Zancolli M, Canevali P, Zocchi MR, Poggi A. Generation of CD4+ or CD8+ regulatory T cells upon mesenchymal stem cell - lymphocyte interaction. Haematologica. 2007;92:881-8. (Pubitemid 350144234)
33. Akle CA, Adinolfi M, Welsh KI, Leibowitz S, McColl I. Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet. 1981;2:1003-5. (Pubitemid 11027574)
34. Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002;30:42-8. (Pubitemid 34059216)
35. Nauta AJ, Westerhuis G, Kruisselbrink AB, Lurvink EG, Willemze R, Fibbe WE. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood. 2006;108: 2114-20. (Pubitemid 44395028)
36. Duthie MS, Reece ST, Lahiri R, Goto W, Raman VS, Kaplan J, et al. Antigen-specifi c cellular and humoral responses are induced by intradermal Mycobacterium leprae infection of the mouse ear. Infect Immun. 2007;75:5290-7. (Pubitemid 350033616)
37. Vukmanovic-Stejic M, Reed JR, Lacy KE, Rustin MH, Akbar AN. Mantoux test as a model for a secondary immune response in humans. Immunol Lett. 2006;107:93-101. (Pubitemid 44779813)
38. Wong DM, Buechner-Maxwell VA, Manning TO, Ward DL. Evaluation of the precision of intradermal injection of control substances for intradermal testing in clinically normal horses. Am J Vet Res. 2005;66:1341-7. (Pubitemid 41613987)
39. Wong DM, Buechner-Maxwell VA, Manning TO, Ward DL. Comparison of results for intradermal testing between clinically normal horses and horses affected with recurrent airway obstruction. Am J Vet Res. 2005;66:1348-55. (Pubitemid 41613988)
40. Bartholemew S, Owens SD, Ferraro GL, Carrade DD, Lara DJ, Librach F, et al. Collection of equine cord blood and placental tissues in forty thoroughbred mares. Equine Vet J. 2009;41:724-8.
41. Banks KL, Greenlee A. Isolation and identifi cation of equine lymphocytes and monocytes. Am J Vet Res. 1981;42:1651-4.
42. McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, et al. The immunogenicity of human adiposederived cells: Temporal changes in vitro. Stem Cells. 2006;24: 1246-53. (Pubitemid 44464693)
43. Najar M, Rouas R, Raicevic G, Boufker HI, Lewalle P, Meuleman N, et al. Mesenchymal stem cells promote or suppress the proliferation of T lymphocytes from cord blood and peripheral blood: The importance of low cell ratio and role of interleukin-6. Cytotherapy. 2009;11:570-83.
44. Bradley LM. Cell proliferation. In: Mishell BB, Shiigi SM. San Francisco: W.H. Freeman and Company; 1980. Selected Methods in Cellular Immunology. p. 153-72.
45. Hodgin EC, McGuire TC, Perryman LE, Grant BD. Evaluation of delayed hypersensitivity responses in normal horses and immunodefi cient foals. Am J Vet Res. 1978;39: 1161-7.
46. Jose-Cunilleras E, Kohn CW, Hillier A, Saville WJ, Lorch G. Intradermal testing in healthy horses and horses with chronic obstructive pulmonary disease, recurrent urticaria, or allergic dermatitis. J Am Vet Med Assoc. 2001;219: 1115-21. (Pubitemid 33607296)
47. Yu J, Zheng C, Ren X, Li J, Liu M, Zhang L, et al. Intravenous administration of bone marrow mesenchymal stem cells benefi ts experimental autoimmune myasthenia gravis mice through an immunomodulatory action. Scand J Immunol. 2010;72:242-9.
48. Crop MJ, Baan CC, Korevaar SS, Ijzermans JN, Alwayn IP, Weimar W, et al. Donor-derived mesenchymal stem cells suppress alloreactivity of kidney transplant patients. Transplantation. 2009;87:896-906.
49. Vidal M, Walker NJ, Napoli E, Borjesson DL. Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue and umbilical cord tissue. Stem Cells Dev. 2011 May 6 [epub ahead of print].
50. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adiposederived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng. 2007;13: 1185-95. (Pubitemid 46986719)
51. 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. (Pubitemid 38019084)