Human mesenchymal stromal cells could deliver erythropoietin and migrate to the basal layer of hair shaft when subcutaneously implanted in a murine model

Tissue and Cell

Volumn 44, Issue 4, 2012, Pages 249-256

  Mok, P L ^a,c   Cheong, S K ^a,b   Leong, C F ^c   Chua, K H ^c   Ainoon, O ^c,d  

^a UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

^b UNIVERSITI TUNKU ABDUL RAHMAN   (Malaysia)

^c DEPARTMENT OF PHARMACOLOGY   (Malaysia)

^d UNIVERSITI SAINS ISLAM MALAYSIA   (Malaysia)

Author keywords

Erythropoietin; Hair regeneration; Hemoglobin; Mesenchymal stromal cells; MIDGE; Nucleofection

Indexed keywords

ERYTHROPOIETIN; HEMOGLOBIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ERYTHROPOIETIN GENE; GENE; GENE CONSTRUCT; GENE EXPRESSION; GENE TARGETING; HAIR; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYMAL STROMA CELL; MINIMALISTIC IMMUNOLOGICALLY DEFINED GENE EXPRESSION CONSTRUCT; MOUSE; NONHUMAN; NUDE MOUSE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; WESTERN BLOTTING;

EUKARYOTA; MURINAE; MUS MUSCULUS; PROKARYOTA;

EID: 84861996223     PISSN: 00408166     EISSN: 15323072     Source Type: Journal    
DOI: 10.1016/j.tice.2012.04.002     Document Type: Article

References (59)

1. Ankrum J., Karp J.M. Mesenchymal stem cell therapy: two steps forward, one step back. Trends Mol. Med. 2010, 16(5):203-209.
2. Bannerman R.M. The mouse in biomedical research. Hematology 1983, vol. II:294-308. Academic Press, New York.
3. Bartholomew A., Patil S., Mackay A., Nelson M., Buyaner D., Hardy W., Mosca J., Sturgeon C., Siatskas M., Mahmud N., Ferrer K., Deans R., Moseley A., Hoffman R., Devine S.M. Baboon mesenchymal stem cells can be genetically modified to secrete human erythropoietin in vivo. Hum. Gene Ther. 2001, 12:1527-1541.
4. Baskin S., Lasker N. Erythropoietin-associated hypertension. N. Engl. J. Med. 1990, 323(14):999.
5. Bell J.B., Aronovich E.L., Schreifels J.M., Beadnell T.C., Hackett P.B. Duration of expression and activity of Sleeping Beauty Transposase in mouse liver following hydrodynamic DNA delivery. Mol. Ther. 2010, 18(10):1796-1802.
6. Bennett C.L., Luminari S., Nissenson A.R., Tallman M.S., Klinge S.A., Mc Williams N., McKoy J.M., Kim B., Lyons E.A., Trifilio S.M., Rasich D.W., Evens A.M., Kuzel T.M., Schumock G.T., Belknap S.M., Locatelli F., Rossert J., Casadevall N. Pure red-cell aplasia and epoetin therapy. N. Engl. J. Med. 2004, 351:1403-1408.
7. Brines M., Cerami A. Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J. Intern. Med. 2008, 264:405-432.
8. Campeau P.M., Rafei M., Fraçois M., Birman E., Forner K., Galipeau J. Mesenchymal stromal cells engineered to express erythropoietin induce anti-erythropoietin antibodies and anemia in allorecipients. Mol. Ther. 2009, 17(2):369-372.
9. Caplan A.I., Bruder S.P. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol. Med. 2001, 7(6):259-263.
10. Choong P.F., Mok P.L., Cheong S.K., Then K.Y. Generating neuron-like cells from BM-derived mesenchymal stromal cells in vitro. Cytotherapy 2007, 9(2):170-183.
11. Choudhri T.F., Hoh B.L., Solomon R.A., Connolly E.S., Pinsky D.J. Use of a spectrophotometric hemoglobin assay to objectively quantify intracerebral hemorrhage in mice. Stroke 1997, 28:2296-2302.
12. Copland I.B., Jolicoeur E.M., Gilis M., Cuerquis J., Eliopoulos N., Annabi B., Calderone A., Tanguay J., Ducharme A., Galipeau J. Coupling erythropoietin secretion to mesenchymal stromal cells enhances their regenerative properties. Cardiovasc. Res. 2008, 79:405-415.
13. Daga A., Muraglia A., Quarto R., Cancedda R., Corte G. Enhanced engraftment of EPO-transduced human bone marrow stromal cells transplanted in a 3D matrix in non-conditioned NOD/SCID mice. Gene Ther. 2002, 9:915-921.
14. Doering C.B. Retroviral modification of mesenchymal stem cells for gene therapy of Hemophilia A. Methods Mol. Biol. 2008, 433(1):203-212.
15. Eckardt K.U. After 15 years of success - perspectives of erythropoietin therapy. Nephrol. Dial. Transplant. 2001, 16:1745-1749.
16. Eliopoulos N., Al-Khaldi A., Crosato M., Lachapelle K., Gallipeau J. A neovascularized organoid derived from retrovirally engineered bone marrow stroma leads to prolonged in vivo systemic delivery of erythropoietin in nonmyeloablated, immunocompetent mice. Nature 2003, 10(6):478-489.
17. Eliopoulos N., Gagnon R.F., Francois M., Gallipeau J. Erythropoietin delivery by genetically engineered bone marrow stromal cells for correction of anemia in mice with chronic renal failure. J. Am. Soc. Nephrol. 2006, 17:1576-1584.
18. Eliopoulos N., Stagg J., Lejeune L., Pommey S., Galipeau J. Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Gene Ther. 2005, 106:4057-4065.
19. Elliott S., Lorenzini T., Asher S., Aoki K., Brankow D., Buck L., Busse L., Chang D., Fuller J., Grant J., Hernday N., Hokum M., Hu S., Knudten A., Levin N., Komorowski R., Martin F., Navarro R., Osslund T., Rogers G., Rogers N., Trail G., Egrie J. Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat. Biotechnol. 2003, 21:414-421.
20. Esneault E., Pacary E., Eddi D., Freret T., Tixier E., Toutain J., Touzani O., Schumann-Bard P., Petit E., Roussel S., Bernaudin M. Combined therapeutic strategy using erythropoietin and mesenchymal stem cells potentiates neurogenesis after transient focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 2008, 28:1552-1563.
21. Fisher J.W. Erythropoietin: physiology and pharmacology update. Exp. Biol. Med. 2003, 228(1):1-14.
22. Ghezzi P., Brines M. Erythropoietin as an antiapoptotic, tissue-protective cytokine. Cell Death Differ. 2004, 11:S37-S44.
23. Gothelf A., Hojman P., Gehl J. Therapeutic levels of erythropoietin (EPO) achieved after gene electrotransfer to skin in mice. Gene Ther. 2010, 17:1077-1084.
24. Grinnemo K.H., Månsson A., Dellgren G., Klingberg D., Wardell E., Drvota V., Tammik C., Holgersson J., Ringdén O., Sylvén C., Le Blanc K. Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium. J. Thorac. Cardiovasc. Surg. 2004, 127:1293-1300.
25. Hamamori Y., Samal B., Tian J., Kedes L. Myoblast transfer of human erythropoietin gene in a mouse model of renal failure. J. Clin. Invest. 1995, 95:1808-1813.
26. Herweijer H., Wolff J.A. Progress and prospects: naked DNA gene transfer and therapy. Gene Ther. 2003, 10:453-458.
27. Hooduijn M.J., Gorjup E., Genever P.G. Comparative characterization of hair follicle dermal stem cells and bone marrow mesenchymal stem cells. Stem Cells Dev. 2006, 15(1):49-60.
28. Jelkmann W. Developments in the therapeutic use of erythropoiesis stimulating agents. Br. J. Haematol. 2008, 141:287-297.
29. Jelkmann W. Erythropoietin: structure, control of production, and function. Physiol. Rev. 1992, 71(s):449-489.
30. Kang S.G., Shinojima N., Hossain A., Gumin J., Yong R.L., Colman H., Marini F., Andreef M., Lang F.F. Erythropoietin promotes hair shaft growth in cultured human hair follicles and modulates hair growth in mice. J. Dermatol. Sci. 2010, 59(2):86-90.
31. Karp J.M., Teo G.S.L. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009, 4(3):206-216.
32. Kato M., Kamiyama H., Okazaki A., Kumaki K., Sugiyama Y. Mechanism for the nonlinear pharmacokinetics of erythropoietin in rats. JPET 1997, 283:520-527.
33. Kim M., O'Callaghan P.M., Droms K.A., James D.C. A mechanistic understanding of production instability in CHO cell lines expressing recombinant monoclonal antibodies. Biotechnol. Bioeng. 2011, 108(10):2434-2446.
34. Kong H., Liu J., Riddle K., Matsumoto T., Leach K., Mooney D.J. Non-viral gene delivery regulated by stiffness of cell adhesion substrates. Nat. Mater. 2005, 4:640-644.
35. Krantz S.B. Erythropoietin. Blood 1991, 77(3):419-434.
36. Lieutaud T., Andrews P.J., Rhodes J.K., Williamson R. Characterization of the pharmacokinetics of human recombinant erythropoietin in blood and brain when administered immediately after lateral fluid percussion brain injury and its pharmacodynamic effects on IL-1 beta and MIP-2 in rats. J. Neurotrauma 2008, 25(10):1179-1185.
37. Lifshitz L., Prutchi-Sagiv S., Avneon M., Gassmann M., Mittelman M., Neumann D. Non-erythroid activities of erythropoietin: functional effects on murine dendritic cells. Mol. Immunol. 2009, 46:713-721.
38. Lifshitz L., Tabak G., Gassmann M., Mittelman M., Neumann D. Macrophages as novel target cells for erythropoietin. Haematologica 2010, 95(1):1823-1831.
39. Liu L.N., Hendricks K., Buyaner D., Boehnlein E., Junker U., Deans R., Vanguri P., Mosca J.D. Systemic erythropoietin expression from human mesenchymal stem cells depend on both cell adherence and delivery route. Abstract in the 6th Annual ISHAGE 2000.
40. Loo M., Beguin Y. The effect of recombinant human erythropoietin on platelet counts is strongly modulated by the adequacy of iron supply. Blood 1999, 93(10):3286-3293.
41. McGinley L., McMahon J., Strappe P., Barry F., Murphy M., O'Toole D., O'Brien T. Lentiviral vector mediated modification of mesenchymal stem cells and enhanced survival in an in vitro model of ischaemia. Stem Cell Res. Ther. 2011, 2:12.
42. Meer P.V.D., Lipsic E., Henning R.H., Boddeus K., van der Velden J., Voors A.A., van Veldhuisen D.J., van Gilst W.H., Schoemaker R.G. Erythropoietin induces neovascularization and improves cardiac function in rats with heart failure after myocardial infarction. J. Am. Coll. Cardiol. 2005, 46(1):125-133.
43. Mok P.L., Cheong S.K., Leong C.F., Chua K.H., Ainoon O. Extended and stable gene expression via nucleofection of MIDGE construct into adult human marrow mesenchymal stromal cells. Cytotechnology 2012, 64:203-216.
44. Mok P.L., Cheong S.K., Leong C.F., Othman A. In vitro expression of erythropoietin by transfected human mesenchymal stromal cells. Cytotherapy 2008, 10(2):116-124.
45. Mok P.L., Leong C.F., Cheong S.K. Isolation and identification of mesenchymal stem cells from human bone marrow. Malays. J. Pathol. 2003, 25(2):121-127.
46. Naldi A.M., Gassmann M., Bodmer D. Erythropoietin but not VEGF has a protective effect on auditory hair cells in the inner ear. Cell. Mol. Life Sci. 2009, 66:3595-3599.
47. Parekkadan B., Milwid J.M. Mesenchymal stem cells as therapeutics. Annu. Rev. Biomed. Eng. 2010, 12:87-117.
48. Schakowski F., Gorschluter M., Junghans C., Schroff M., Buttgereit P., Ziske C., Schöttker B., König-Merediz S.A., Sauerbruch T., Wittig B., Schmidt-Wolf I.G. A novel minimal-size vector (MIDGE) improves transgene expression in colon carcinoma cells and avoids transfections of undesired DNA. Mol. Ther. 2001, 3:793-800.
49. Singer N.G., Caplan A.I. Mesenchymal stem cells: mechanisms of inflammation. Annu. Rev. Pathol. Mech. Dis. 2011, 6:457-478.
50. Stenn K., Parimoo S., Zheng Y., Barrows T., Washenik K. Bioengineering the hair follicle. Organogenesis 2007, 3(1):6-13.
51. Terrovitis J.V., Smith R.R., Marbán E. Assessment and optimization of cell engraftment after transplantation into the heart. Circ. Res. 2010, 106:479-494.
52. Toma C., Pittenger M.F., Cahill K.S., Byrne B.J., Kessler P.D. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 2002, 105(1):93-98.
53. Tomita M., Adachi Y., Yamada H., Takahashi K., Kiuchi K., Oyaizy H., Ikekuburo K., Kaneda H., Matsumura M., Ikehara S. Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells 2002, 20:279-283.
54. Tsakiris D. Morbidity and mortality reduction associated with the use of erythropoietin. Nephron 2000, 85(Suppl. 1):2-8.
55. Tse W.T., Pendleton J.D., Beyer W.M., Egalka M.C., Guinan E.C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003, 75(3):389-397.
56. Wang G., Liu L.N., Lee K., Buyaner D., Hendricks K., Kalfoglou C.S., Bohnlein E., Junker U., Mosca J.D. Comparison of drug and cell-based delivery-engineering adult mesenchymal stem cells to deliver human erythropoietin. Gene Ther. Mol. Biol. 2009, 13:321-330.
57. Wong C.Y., Cheong S.K., Mok P.L., Leong C.F. Differentiation of human mesenchymal stem cells into mesangial cells in post-glomerular injury murine model. Pathology 2008, 40(1):52-57.
58. Yoo B.Y., Shin Y.H., Yoon H.H., Seo Y.K., Park J.K. Application of mesenchymal stem cells derived from bone marrow and umbilical cord in human hair multiplication. J. Dermatol. Sci. 2010, 60:74-83.
59. Zhang D., Zhang F., Zhang Y., Gao X., Li C., Yang N., Cao K. Combining erythropoietin infusion with intramyocardial delivery of bone marrow cells is more effective for cardiac repair. Transpl. Int. 2007, 20(2):174-183.