Bone marrow stem cell applied in the canine veterinary clinics

Cell therapy represents an old therapeutic practice initiated with the transfusion of whole blood in different clinical situations. There is now a breakthrough in the study of multipotent stem cell therapy because of its functionality in regeneration of tissues, which promotes attention of the scientific community. Bone marrow is one of the main sources of multipotent stem cells, composed by hematopoietic stem cells responsible for the renewal of the cellular components of the blood, and mesenchymal stem cells that aid in the regeneration of tissues. These cells have a strong potential for the treatment of several diseases, due their main characteristics such as high plasticity, capacity for self-renewal and immunomodulation. Although, there are many studies that show good results with the use of cell therapy as a form of treatment for several diseases, some studies still show inconclusive or unsatisfactory results. Therefore, the objective of this study was to review the application of bone marrow stem cells in the canine model since improvements on the knowledge of the technique are necessary to enable its applicability with safety and efficacy.

INDEX TERMS:
Stem cells; bone marrow; hematopoietic; dogs

Authorship

Ingrid S. Gomes

Departamento de Medicina Veterinária, Faculdade de Zootecnia e Tecnologia Alimentar (FZEA), Universidade de São Paulo (USP), Av. Duque de Caxias Norte 255, Pirassununga, SP 13635-900, Brazil.Universidade de São PauloBrazilPirassununga, SP, BrazilDepartamento de Medicina Veterinária, Faculdade de Zootecnia e Tecnologia Alimentar (FZEA), Universidade de São Paulo (USP), Av. Duque de Caxias Norte 255, Pirassununga, SP 13635-900, Brazil.

Vanessa C. de Oliveira

Departamento de Cirurgia, FMVZ-USP, Av. Duque de Caxias Norte 255, Pirassununga, SP 13635-900, Brazil.USPBrazilPirassununga, SP, BrazilDepartamento de Cirurgia, FMVZ-USP, Av. Duque de Caxias Norte 255, Pirassununga, SP 13635-900, Brazil.

Alessandra O. Pinheiro

Kelly C.S.Roballo ^**Corresponding author: kellyroballo@gmail.com

Giuliano S.M. de Araujo

Jessica C. Veronezi

Daniele S. Martins

Carlos Eduardo Ambrósio

*Corresponding author: kellyroballo@gmail.com

Conflict of interest statement.- The authors have no competing interests.

SCIMAGO INSTITUTIONS RANKINGS

Figures

Figures (2)

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Fig.1.
Studies performed in the last years on hematopoietic stem cells from canine bone marrow. (Osgood et al. 1939Osgood E.E., Riddle M.C. & Mathews T.J. 1939. Aplastic anemia treated with daily transfusions and intravenous marrow: case report. Ann. Intern. Med. 13:357-367., Thomas et al. 1962Thomas E.D., Collins J.A., Hernan Jr E.C. & Ferrebee J.W. 1962. Marrow transplantations in lethally irradiated dogs given methotrexate. Blood 19:217-28., Epstein et al. 1967Epstein R.B., Bryant J. & Thomas E.D. 1967. Cytogenetic demonstration of permanent tolerance in adult outbred dogs. Transplantation 5:267-272., Escobar et al. 2012Escobar C., Grindem C., Neel J.A. & Suter S.E. 2012. Hematologic changes after total body irradiation and autologous transplantation of hematopoietic peripheral blood progenitor cells in dogs with lymphoma. Vet. Pathol. 49(2):341-343., Killian et al. 2013Killian D., Reichard M., Knueppel A., Lange S., Sekora A., Knuebel G., Murua E.H., Guthoff R., Stachs O. & Junghanss C. 2013. Distribution changes of epithelial dendritic cells in canine cornea and mucous membranes related to hematopoietic stem cell transplantation. In Vivo 27(6):761-771., Sato et al. 2013Sato M., Storb R., Loretz C., Stone D., Mielcarek M., Sale G.E., Rezvani A.R. & Graves S.S. 2013. Inducible costimulator (ICOS) up-regulation on activated T cells in chronic graft-versus-host disease after dog leukocyte antigen-nonidentical hematopoietic cell transplantation: a potential therapeutic target. Transplantation 96(1):34-41., Mathes et al. 2014Mathes D.W., Chang J., Hwang B., Graves S.S., Storer B.E., Butts-Miwongtum T., Venda G.E. & Storb R. 2014. Simultaneous transplantation of hematopoietic stem cells and a vascularized composite allograft leads to tolerance. Transplantatin 98(2):131-138., Vrecenak et al. 2014Vrecenak J.D., Pearson E.G., Santore M.T., Todorow C.A., Li H., Radu A., Bhatti T., Peranteau W.H., Johnson M.P. & Flake A.W. 2014. Stable long-term mixed chimerism achieved in a canine model of allogeneic in utero hematopoietic cell transplantation. Blood 124(12):1987-95., Rosinski et al. 2015Rosinski S.L., Stone B., Graves S.S., Fuller D.H., De Rosa S.C., Spies G.A., Mize G.J., Fuller J.T. & Storb R. 2015. Development of a minor histocompatibility antigen vaccine regimen in the canine model of hematopoietic cell transplantation. Transplantation 99(10):2083-2094., Suter et al. 2015Suter S.E., Hamilton M.J., Sullivan E.W. & Venkataraman G.M. 2015. Allogeneic hematopoietic cell transplantation in a dog with acute large granular lymphocytic leukemia. J. Am. Vet. Med. Assoc. 246(9):994-947., Luangphakdy et al. 2016Luangphakdy V., Boehm C., Pan H., Herrick J., Zaveri P. & Muschler G.F. 2016. Assessment of methods for rapid intraoperative concentration and selection of marrow-derived connective tissue progenitors for bone regeneration using the canine femoral multidefect model. Tissue Eng. A 22(1/2):17-30., Lange et al. 2017Lange S., Steder A., Killian D., Knuebel G., Sekora A., Vogel H., Lindner I., Dunkelmann S., Prall F., Escobar H.M., Freund M. & Junghanss C. 2017. Engraftment efficiency after intra-bone marrow versus intravenous transplantation of bone marrow cells in a canine nonmyeloablative dog leukocyte antigen-identical transplantation model. Biol. Blood Marrow Transplant. 23(2):247-254.)

Thumbnail

Fig.2.
Studies performed in the last years on mesenchymal stem cells from canine bone marrow. (Friedenstein et al. 1974Friedenstein A.J., Chailakhyan R.K., Latsinik N.V., Panasyuk A.F. & Keiliss-Borok I.V. 1974. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17:331-340., Tharasanit et al. 2011Tharasanit T., Phuticanit N., Wangdee C., Soontornvipart K., Tantrajak S., Kaewamatawong T., Suwimonteerabutr J., Supaphol P. & Techakumphu M. 2011. Differentiation potentials of canine bone marrow mesenchymal stem cells. J. Vet. Med. 41(1):79-86., Rici et al. 2012Rici R.E., Alcantara D., Fratini P., Wenceslau C.V., Ambrosio C.E., Miglino M.A. & Maria D.A. 2012. Mesenchymal stem cells with rhBMP-2 inhibits the growth of canine osteosarcoma cells. BMC Vet. Res. 8:17., Kim et al. 2013Kim J.K., Lee J.H., Lyoo Y.S., Jung D.I. & Park H.M. 2013. The effects of topical mesenchymal stem cell transplantation in canine experimental cutaneous wounds. Vet. Dermatol. 24(2):242-253., Hu et al. 2014Hu Y.C., Liu X., Shen J.J., He J.C. & Chen Q.E. 2014. Experimental study of canine bone marrow mesenchymal stem cells combined with calcium phosphate cement for repair of mandibular bone defects in Beagle dogs. Shanghai Kou Qiang Yi Xue 23(4):402-408., Besalt et al. 2015Besalti O., Can P., Akpinar E., Aktas Z., Elcin A.E. & Elcin Y.M. 2015. Intraspinal transplantation of autologous neurogenically-induced bone marrow-derived mesenchymal stem cells in the treatment of paraplegic dogs without deep pain perception secondary to intervertebral disk disease. Turk Neurosurg. 25(4):625-632., Guo et al. 2015Guo P., Zeng J.J. & Zhou N. 2015. A novel experimental study on the fabrication and biological characteristics of canine bone marrow mesenchymal stem cells sheet using vitamin C. Scanning 37(1):42-48., Hao et al. 2015Hao L., Hao J., Fang W., Han C., Zhang K. & Wang X. 2015. Dual isotope simultaneous imaging to evaluate the effects of intracoronary bone marrow-derived mesenchymal stem cells on perfusion and metabolism in canines with acute myocardial infarction. Biomed. Rep. 3(4): 447-452., Lim et al. 2016Lim C.Y., Han J.I., Kim S.G., Lee C.M. & Parque H.M. 2016. Evaluation of autologous bone marrow-derived mesenchymal stem cells on renal regeneration after experimentally induced acute kidney injury in dogs. Am. J. Vet. Res. 77(4):403., Das et al. 2017Das K., Mili B., Madhusoodan A.P., Saxena A.C., Kumar A., Singh P., Verma M.R., Sarkar M. & Bag S. 2017. Proliferation of canine bone marrow derived mesenchymal stem cells on different nanomaterial based thin film scaffolds. Tissue Cell; doi: http://dx.doi.org/10.1016/j.tice.2017.02.002
https://doi.org/10.1016/j.tice.2017.02.0... )

Fig.1. Studies performed in the last years on hematopoietic stem cells from canine bone marrow. (Osgood et al. 1939Osgood E.E., Riddle M.C. & Mathews T.J. 1939. Aplastic anemia treated with daily transfusions and intravenous marrow: case report. Ann. Intern. Med. 13:357-367., Thomas et al. 1962Thomas E.D., Collins J.A., Hernan Jr E.C. & Ferrebee J.W. 1962. Marrow transplantations in lethally irradiated dogs given methotrexate. Blood 19:217-28., Epstein et al. 1967Epstein R.B., Bryant J. & Thomas E.D. 1967. Cytogenetic demonstration of permanent tolerance in adult outbred dogs. Transplantation 5:267-272., Escobar et al. 2012Escobar C., Grindem C., Neel J.A. & Suter S.E. 2012. Hematologic changes after total body irradiation and autologous transplantation of hematopoietic peripheral blood progenitor cells in dogs with lymphoma. Vet. Pathol. 49(2):341-343., Killian et al. 2013Killian D., Reichard M., Knueppel A., Lange S., Sekora A., Knuebel G., Murua E.H., Guthoff R., Stachs O. & Junghanss C. 2013. Distribution changes of epithelial dendritic cells in canine cornea and mucous membranes related to hematopoietic stem cell transplantation. In Vivo 27(6):761-771., Sato et al. 2013Sato M., Storb R., Loretz C., Stone D., Mielcarek M., Sale G.E., Rezvani A.R. & Graves S.S. 2013. Inducible costimulator (ICOS) up-regulation on activated T cells in chronic graft-versus-host disease after dog leukocyte antigen-nonidentical hematopoietic cell transplantation: a potential therapeutic target. Transplantation 96(1):34-41., Mathes et al. 2014Mathes D.W., Chang J., Hwang B., Graves S.S., Storer B.E., Butts-Miwongtum T., Venda G.E. & Storb R. 2014. Simultaneous transplantation of hematopoietic stem cells and a vascularized composite allograft leads to tolerance. Transplantatin 98(2):131-138., Vrecenak et al. 2014Vrecenak J.D., Pearson E.G., Santore M.T., Todorow C.A., Li H., Radu A., Bhatti T., Peranteau W.H., Johnson M.P. & Flake A.W. 2014. Stable long-term mixed chimerism achieved in a canine model of allogeneic in utero hematopoietic cell transplantation. Blood 124(12):1987-95., Rosinski et al. 2015Rosinski S.L., Stone B., Graves S.S., Fuller D.H., De Rosa S.C., Spies G.A., Mize G.J., Fuller J.T. & Storb R. 2015. Development of a minor histocompatibility antigen vaccine regimen in the canine model of hematopoietic cell transplantation. Transplantation 99(10):2083-2094., Suter et al. 2015Suter S.E., Hamilton M.J., Sullivan E.W. & Venkataraman G.M. 2015. Allogeneic hematopoietic cell transplantation in a dog with acute large granular lymphocytic leukemia. J. Am. Vet. Med. Assoc. 246(9):994-947., Luangphakdy et al. 2016Luangphakdy V., Boehm C., Pan H., Herrick J., Zaveri P. & Muschler G.F. 2016. Assessment of methods for rapid intraoperative concentration and selection of marrow-derived connective tissue progenitors for bone regeneration using the canine femoral multidefect model. Tissue Eng. A 22(1/2):17-30., Lange et al. 2017Lange S., Steder A., Killian D., Knuebel G., Sekora A., Vogel H., Lindner I., Dunkelmann S., Prall F., Escobar H.M., Freund M. & Junghanss C. 2017. Engraftment efficiency after intra-bone marrow versus intravenous transplantation of bone marrow cells in a canine nonmyeloablative dog leukocyte antigen-identical transplantation model. Biol. Blood Marrow Transplant. 23(2):247-254.)

Fig.2. Studies performed in the last years on mesenchymal stem cells from canine bone marrow. (Friedenstein et al. 1974Friedenstein A.J., Chailakhyan R.K., Latsinik N.V., Panasyuk A.F. & Keiliss-Borok I.V. 1974. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17:331-340., Tharasanit et al. 2011Tharasanit T., Phuticanit N., Wangdee C., Soontornvipart K., Tantrajak S., Kaewamatawong T., Suwimonteerabutr J., Supaphol P. & Techakumphu M. 2011. Differentiation potentials of canine bone marrow mesenchymal stem cells. J. Vet. Med. 41(1):79-86., Rici et al. 2012Rici R.E., Alcantara D., Fratini P., Wenceslau C.V., Ambrosio C.E., Miglino M.A. & Maria D.A. 2012. Mesenchymal stem cells with rhBMP-2 inhibits the growth of canine osteosarcoma cells. BMC Vet. Res. 8:17., Kim et al. 2013Kim J.K., Lee J.H., Lyoo Y.S., Jung D.I. & Park H.M. 2013. The effects of topical mesenchymal stem cell transplantation in canine experimental cutaneous wounds. Vet. Dermatol. 24(2):242-253., Hu et al. 2014Hu Y.C., Liu X., Shen J.J., He J.C. & Chen Q.E. 2014. Experimental study of canine bone marrow mesenchymal stem cells combined with calcium phosphate cement for repair of mandibular bone defects in Beagle dogs. Shanghai Kou Qiang Yi Xue 23(4):402-408., Besalt et al. 2015Besalti O., Can P., Akpinar E., Aktas Z., Elcin A.E. & Elcin Y.M. 2015. Intraspinal transplantation of autologous neurogenically-induced bone marrow-derived mesenchymal stem cells in the treatment of paraplegic dogs without deep pain perception secondary to intervertebral disk disease. Turk Neurosurg. 25(4):625-632., Guo et al. 2015Guo P., Zeng J.J. & Zhou N. 2015. A novel experimental study on the fabrication and biological characteristics of canine bone marrow mesenchymal stem cells sheet using vitamin C. Scanning 37(1):42-48., Hao et al. 2015Hao L., Hao J., Fang W., Han C., Zhang K. & Wang X. 2015. Dual isotope simultaneous imaging to evaluate the effects of intracoronary bone marrow-derived mesenchymal stem cells on perfusion and metabolism in canines with acute myocardial infarction. Biomed. Rep. 3(4): 447-452., Lim et al. 2016Lim C.Y., Han J.I., Kim S.G., Lee C.M. & Parque H.M. 2016. Evaluation of autologous bone marrow-derived mesenchymal stem cells on renal regeneration after experimentally induced acute kidney injury in dogs. Am. J. Vet. Res. 77(4):403., Das et al. 2017Das K., Mili B., Madhusoodan A.P., Saxena A.C., Kumar A., Singh P., Verma M.R., Sarkar M. & Bag S. 2017. Proliferation of canine bone marrow derived mesenchymal stem cells on different nanomaterial based thin film scaffolds. Tissue Cell; doi: http://dx.doi.org/10.1016/j.tice.2017.02.002
https://doi.org/10.1016/j.tice.2017.02.0... )

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Colégio Brasileiro de Patologia Animal - CBPA Pesquisa Veterinária Brasileira, Caixa Postal 74.591, 23890-000 Rio de Janeiro, RJ, Brasil, Tel./Fax: (55 21) 2682-1081 - Rio de Janeiro - RJ - Brazil
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[1] *Corresponding author: kellyroballo@gmail.com