Comparative phenotypic and molecular characterization of porcine mesenchymal stem cells from different sources for translational studies in a large animal model

Veterinary Immunology and Immunopathology

Volumn 147, Issue 1-2, 2012, Pages 104-112

  Casado, Javier G ^a   Gomez Mauricio, G ^a   Alvarez, V ^a   Mijares, J ^a   Tarazona, R ^b   Bernad, A ^c   Sanchez Margallo, F M ^a  

^a JESÚS USÓN MINIMALLY INVASIVE SURGERY CENTRE   (Spain)

^b UNIVERSITY OF EXTREMADURA   (Spain)

^c CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

Large animal model; Mesenchymal stem cells; Phenotypic analysis; QRT PCR

Indexed keywords

CD11B ANTIGEN; CD18 ANTIGEN; CD61 ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ADIPOSE DERIVED STEM CELL; ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL SURFACE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; MESENCHYMAL STEM CELL; NONHUMAN; PERIPHERAL BLOOD STEM CELL; PHENOTYPIC VARIATION; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL EXPANSION; SWINE; TRANSLATIONAL RESEARCH;

ADIPOGENESIS; ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CHONDROGENESIS; HUMANS; MESENCHYMAL STROMAL CELLS; MODELS, ANIMAL; OSTEOGENESIS; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; SWINE; TRANSLATIONAL MEDICAL RESEARCH;

ANIMALIA; SUIDAE; SUS;

EID: 84860917300     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2012.03.015     Document Type: Article

References (60)

1. Annenkov A. The insulin-like growth factor (IGF) receptor type 1 (IGF1R) as an essential component of the signalling network regulating neurogenesis. Mol. Neurobiol. 2009, 40:195-215.
2. Arinzeh T.L. Mesenchymal stem cells for bone repair: preclinical studies and potential orthopedic applications. Foot Ankle Clin. 2005, 10:651-665. viii.
3. bdel-Mageed A.S., Senagore A.J., Pietryga D.W., Connors R.H., Giambernardi T.A., Hay R.V., Deng W. Intravenous administration of mesenchymal stem cells genetically modified with extracellular superoxide dismutase improves survival in irradiated mice. Blood 2009, 113:1201-1203.
4. Cao H., Chu Y., Zhu H., Sun J., Pu Y., Gao Z., Yang C., Peng S., Dou Z., Hua J. Characterization of immortalized mesenchymal stem cells derived from foetal porcine pancreas. Cell Prolif. 2011, 44:19-32.
5. Casal M., Haskins M. Large animal models and gene therapy. Eur. J. Hum. Genet. 2006, 14:266-272.
6. Chamberlain G., Smith H., Rainger G.E., Middleton J. Mesenchymal stem cells exhibit firm adhesion, crawling, spreading and transmigration across aortic endothelial cells: effects of chemokines and shear. PLoS One 2011, 6:e25663.
7. Comite P., Cobianchi L., Avanzini M.A., Zonta S., Mantelli M., Achille V., De M.M., Cansolino L., Ferrari C., Alessiani M., Maccario R., Gandolfo G.M., Dionigi P., Locatelli F., Bernardo M.E. Isolation and ex vivo expansion of bone marrow-derived porcine mesenchymal stromal cells: potential for application in an experimental model of solid organ transplantation in large animals. Transplant. Proc. 2010, 42:1341-1343.
8. de Mattos C.A., Alves A.L., Golim M.A., Moroz A., Hussni C.A., de Oliveira P.G., Deffune E. Isolation and immunophenotypic characterization of mesenchymal stem cells derived from equine species adipose tissue. Vet. Immunol. Immunopathol. 2009, 132:303-306.
9. DelaRosa O., Lombardo E., Beraza A., Mancheno-Corvo P., Ramirez C., Menta R., Rico L., Camarillo E., Garcia L., Abad J.L., Trigueros C., Delgado M., Buscher D. Requirement of IFN-gamma-mediated indoleamine 2,3-dioxygenase expression in the modulation of lymphocyte proliferation by human adipose-derived stem cells. Tissue Eng. A 2009, 15:2795-2806.
10. DelaRosa O., Sanchez-Correa B., Morgado S., Ramirez C., Del R.B., Menta R., Lombardo E., Tarazona R., Casado J.G. Human adipose-derived stem cells impair NK cell function and exhibit low susceptibility to NK-mediated lysis. Stem Cells Dev. 2011, 10.1089/scd.2011.0139.
11. Fang B., Song Y., Zhao R.C., Han Q., Lin Q. Using human adipose tissue-derived mesenchymal stem cells as salvage therapy for hepatic graft-versus-host disease resembling acute hepatitis. Transplant. Proc. 2007, 39:1710-1713.
12. Fukui M., Zhu B.T. Mitochondrial superoxide dismutase SOD2, but not cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells. Free Radic. Biol. Med. 2010, 48:821-830.
13. Garcia-Olmo D., Herreros D., Pascual I., Pascual J.A., Del-Valle E., Zorrilla J., De-La-Quintana P., Garcia-Arranz M., Pascual M. Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial. Dis. Colon Rectum 2009, 52:79-86.
14. Gonzalez-Rey E., Anderson P., Gonzalez M.A., Rico L., Buscher D., Delgado M. Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 2009, 58:929-939.
15. Gonzalez-Rey E., Gonzalez M.A., Varela N., O'Valle F., Hernandez-Cortes P., Rico L., Buscher D., Delgado M. Human adipose-derived mesenchymal stem cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann. Rheum. Dis. 2010, 69:241-248.
16. Gupta R., Karpatkin S., Basch R.S. Hematopoiesis and stem cell renewal in long-term bone marrow cultures containing catalase. Blood 2006, 107:1837-1846.
17. Hegab A.E., Kubo H., Fujino N., Suzuki T., He M., Kato H., Yamaya M. Isolation and characterization of murine multipotent lung stem cells. Stem Cells Dev. 2010, 19:523-536.
18. Hernandeza J., Torres-Espina A., Navarro X. Adult stem cell transplants for spinal cord injury repair: current state in preclinical research. Curr. Stem Cell Res. Ther. 2011, 6:273-287.
19. Jaiswal N., Haynesworth S.E., Caplan A.I., Bruder S.P. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J. Cell Biochem. 1997, 64:295-312.
20. Janssens S. Stem cells in the treatment of heart disease. Annu. Rev. Med. 2010, 61:287-300.
21. Joers V.L., Emborg M.E. Preclinical assessment of stem cell therapies for neurological diseases. ILAR J. 2009, 51:24-41.
22. Josiah D.T., Zhu D., Dreher F., Olson J., McFadden G., Caldas H. Adipose-derived stem cells as therapeutic delivery vehicles of an oncolytic virus for glioblastoma. Mol. Ther. 2010, 18:377-385.
23. Karussis D., Kassis I. The potential use of stem cells in multiple sclerosis: an overview of the preclinical experience. Clin. Neurol. Neurosurg. 2008, 110:889-896.
24. Kawaguchi N., Smith A.J., Waring C.D., Hasan M.K., Miyamoto S., Matsuoka R., Ellison G.M. c-kitpos GATA-4 high rat cardiac stem cells foster adult cardiomyocyte survival through IGF-1 paracrine signalling. PLoS One 2010, 5:e14297.
25. King M., Pearson T., Rossini A.A., Shultz L.D., Greiner D.L. Humanized mice for the study of type 1 diabetes and beta cell function. Ann. N. Y. Acad. Sci. 2008, 1150:46-53.
26. Klammt J., Kiess W., Pfaffle R. IGF1R mutations as cause of SGA. Best. Pract. Res. Clin. Endocrinol. Metab. 2011, 25:191-206.
27. Kondo K., Shintani S., Shibata R., Murakami H., Murakami R., Imaizumi M., Kitagawa Y., Murohara T. Implantation of adipose-derived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:61-66.
28. Kumar B.M., Yoo J.G., Ock S.A., Kim J.G., Song H.J., Kang E.J., Cho S.K., Lee S.L., Cho J.H., Balasubramanian S., Rho G.J. In vitro differentiation of mesenchymal progenitor cells derived from porcine umbilical cord blood. Mol. Cells 2007, 24:343-350.
29. Lee S.T., Chu K., Jung K.H., Im W.S., Park J.E., Lim H.C., Won C.H., Shin S.H., Lee S.K., Kim M., Roh J.K. Slowed progression in models of Huntington disease by adipose stem cell transplantation. Ann. Neurol. 2009, 66:671-681.
30. Lin T.Y., Rush L.J., London C.A. Generation and characterization of bone marrow-derived cultured canine mast cells. Vet. Immunol. Immunopathol. 2006, 113:37-52.
31. Lin G., Wang G., Liu G., Yang L.J., Chang L.J., Lue T.F., Lin C.S. Treatment of type 1 diabetes with adipose tissue-derived stem cells expressing pancreatic duodenal homeobox 1. Stem Cells Dev. 2009, 18:1399-1406.
32. Liu S.H., Huang J.P., Lee R.K., Huang M.C., Wu Y.H., Chen C.Y., Chen C.P. Paracrine factors from human placental multipotent mesenchymal stromal cells protect endothelium from oxidative injury via STAT3 and manganese superoxide dismutase activation. Biol. Reprod. 2010, 82:905-913.
33. Liu Y., Wang L., Fatahi R., Kronenberg M., Kalajzic I., Rowe D., Li Y., Maye P. Isolation of murine bone marrow derived mesenchymal stem cells using Twist2 Cre transgenic mice. Bone 2010, 47:916-925.
34. Lo B., Kriegstein A., Grady D. Clinical trials in stem cell transplantation: guidelines for scientific and ethical review. Clin. Trials 2008, 5:517-522.
35. Lukacs R.U., Goldstein A.S., Lawson D.A., Cheng D., Witte O.N. Isolation, cultivation and characterization of adult murine prostate stem cells. Nat. Protoc. 2010, 5:702-713.
36. Mackay A.M., Beck S.C., Murphy J.M., Barry F.P., Chichester C.O., Pittenger M.F. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng. 1998, 4:415-428.
37. Mafi P., Hindocha S., Mafi R., Griffin M., Khan W.S. Adult mesenchymal stem cells and cell surface characterization - a systematic review of the literature. Open Orthop. J. 2011, 5:253-260.
38. Martin S.D., Collier F.M., Kirkland M.A., Walder K., Stupka N. Enhanced proliferation of human skeletal muscle precursor cells derived from elderly donors cultured in estimated physiological (5%) oxygen. Cytotechnology 2009, 61:93-107.
39. Matthay M.A., Goolaerts A., Howard J.P., Lee J.W. Mesenchymal stem cells for acute lung injury: preclinical evidence. Crit. Care Med. 2010, 38:S569-S573.
40. Mizuno H. Adipose-derived stem and stromal cells for cell-based therapy: current status of preclinical studies and clinical trials. Curr. Opin. Mol. Ther. 2010, 12:442-449.
41. Ock S.A., Jeon B.G., Rho G.J. Comparative characterization of porcine mesenchymal stem cells derived from bone marrow extract and skin tissues. Tissue Eng. C: Methods 2010, 16:1481-1491.
42. Park B.W., Kang D.H., Kang E.J., Byun J.H., Lee J.S., Maeng G.H., Rho G.J. Peripheral nerve regeneration using autologous porcine skin-derived mesenchymal stem cells. J. Tissue Eng. Regen. Med. 2011, 10.1002/term.404.
43. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
44. Polisetty N., Fatima A., Madhira S.L., Sangwan V.S., Vemuganti G.K. Mesenchymal cells from limbal stroma of human eye. Mol. Vis. 2008, 14:431-442.
45. Quraishi A., Losordo D.W. Ischemic tissue repair by autologous bone marrow-derived stem cells: scientific basis and preclinical data. Handbook of Experimental Pharmacology 2007, pp. 167-179.
46. Ranera B., Lyahyai J., Romero A., Vazquez F.J., Remacha A.R., Bernal M.L., Zaragoza P., Rodellar C., Martin-Burriel I. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue. Vet. Immunol. Immunopathol. 2011, 144:147-154.
47. Riordan N.H., Ichim T.E., Min W.P., Wang H., Solano F., Lara F., Alfaro M., Rodriguez J.P., Harman R.J., Patel A.N., Murphy M.P., Lee R.R., Minev B. Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J. Transl. Med. 2009, 7:29.
48. Ryu H.H., Lim J.H., Byeon Y.E., Park J.R., Seo M.S., Lee Y.W., Kim W.H., Kang K.S., Kweon O.K. Functional recovery and neural differentiation after transplantation of allogenic adipose-derived stem cells in a canine model of acute spinal cord injury. J. Vet. Sci. 2009, 10:273-284.
49. Shimaya M., Muneta T., Ichinose S., Tsuji K., Sekiya I. Magnesium enhances adherence and cartilage formation of synovial mesenchymal stem cells through integrins. Osteoarthritis Cartilage 2010, 18:1300-1309.
50. Shizuru J.A., Negrin R.S., Weissman I.L. Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu. Rev. Med. 2005, 56:509-538.
51. Singla D.K. Stem cells in the infarcted heart. J. Cardiovasc. Transl. Res. 2010, 3:73-78.
52. Taxonera C., Schwartz D.A., Garcia-Olmo D. Emerging treatments for complex perianal fistula in Crohn's disease. World J. Gastroenterol. 2009, 15:4263-4272.
53. Trottier V., Marceau-Fortier G., Germain L., Vincent C., Fradette J. IFATS collection: using human adipose-derived stem/stromal cells for the production of new skin substitutes. Stem Cells 2008, 26:2713-2723.
54. Vlasits J., Jakopitsch C., Bernroitner M., Zamocky M., Furtmuller P.G., Obinger C. Mechanisms of catalase activity of heme peroxidases. Arch. Biochem. Biophys. 2010, 500:74-81.
55. Wang X., Moutsoglou D. Osteogenic and adipogenic differentiation potential of an immortalized fibroblast-like cell line derived from porcine peripheral blood. In Vitro Cell Dev. Biol. Anim. 2009, 45:584-591.
56. Wang K.H., Kao A.P., Wangchen H., Wang F.Y., Chang C.H., Chang C.C., Lin S.D. Optimizing proliferation and characterization of multipotent stem cells from porcine adipose tissue. Biotechnol. Appl. Biochem. 2008, 51:159-166.
57. Wijewardana V., Sugiura K., Shigeyama N., Moriguchi M., Tsunoda S., Ikehara S., Inaba T. Isolation and characterization of hematopoietic progenitor cells in canine bone marrow. Vet. Immunol. Immunopathol. 2007, 115:230-238.
58. Williams K.J., Picou A.A., Kish S.L., Giraldo A.M., Godke R.A., Bondioli K.R. Isolation and characterization of porcine adipose tissue-derived adult stem cells. Cells Tissues Organs 2008, 188:251-258.
59. Williams K.J., Godke R.A., Bondioli K.R. Isolation and culture of porcine adipose tissue-derived somatic stem cells. Methods Mol. Biol. 2011, 702:77-86.
60. Yu G., Wu X., Kilroy G., Halvorsen Y.D., Gimble J.M., Floyd Z.E. Isolation of murine adipose-derived stem cells. Methods Mol. Biol. 2011, 702:29-36.