A comparison of the reparative and angiogenic properties of mesenchymal stem cells derived from the bone marrow of BALB/c and C57/BL6 mice in a model of limb ischemia

Stem Cell Research and Therapy

Volumn 4, Issue 4, 2013, Pages

  Cunha, Flavia Franco ^a   Martins, Leonardo ^a   Martin, Priscila Keiko Matsumoto ^a   Stilhano, Roberta Sessa ^a   Han, Sang Won ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Angiogenesis; Cell therapy; Hind limb ischemia; Mesenchymal stem cells

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; BONE MARROW CELL; C57BL MOUSE; CAPILLARY DENSITY; CELL INFILTRATION; CELL REGENERATION; CELL THERAPY; CHROMOSOME 7; COMPARATIVE STUDY; CONTROLLED STUDY; FIBROSIS; GASTROCNEMIUS MUSCLE; GENETIC DIFFERENCE; HISTOPATHOLOGY; IN VIVO STUDY; INJECTION; LIMB ISCHEMIA; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; OUTCOME ASSESSMENT; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURIFICATION; TISSUE NECROSIS; TISSUE REGENERATION; ANIMAL; BIOLOGICAL THERAPY; BONE MARROW; DISEASE MODEL; ENDOTHELIUM CELL; HINDLIMB; ISCHEMIA; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; VASCULARIZATION;

ANIMALIA; MUS;

ANIMALS; BONE MARROW; CELL- AND TISSUE-BASED THERAPY; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HINDLIMB; ISCHEMIA; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 84880943141     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt245     Document Type: Article

References (59)

1. Critical limb ischemia. Gresele P, Busti C, Fierro T, Intern Emerg Med 2011 6 129 134 22009625
2. Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II). Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG, Bell K, Caporusso J, Durand-Zaleski I, Komori K, Lammer J, Liapis C, Novo S, Razavi M, Robbs J, Schaper N, Shigematsu H, Sapoval M, White C, White J, Clement D, Creager M, Jaff M, Mohler E, Rutherford RB 3rd, Sheehan P, Sillesen H, Rosenfield K, TASC II Working Group, Eur J Vasc Endovasc Surg 2007 33 1 S75 10.1016/j.ejvs.2006.09.024 17140820 (Pubitemid 46068992)
3. Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Scholz D, Cai WJ, Schaper W, Angiogenesis 2001 4 247 257 10.1023/A:1016094004084 12197469 (Pubitemid 34832369)
4. Multilineage potential of adult human mesenchymal stem cells. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR, Science 1999 284 143 147 10.1126/science.284.5411.143 10102814 (Pubitemid 29282067)
5. Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Dezawa M, Ishikawa H, Itokazu Y, Yoshihara T, Hoshino M, Takeda S, Ide C, Nabeshima Y, Science 2005 309 314 317 10.1126/science.1110364 16002622 (Pubitemid 40967871)
6. Contribution of human bone marrow stem cells to individual skeletal myotubes followed by myogenic gene activation. Lee JH, Kosinski PA, Kemp DM, Exp Cell Res 2005 307 174 182 10.1016/j.yexcr.2005.03.008 15922737 (Pubitemid 40732743)
7. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Al-Khaldi A, Eliopoulos N, Martineau D, Lejeune L, Lachapelle K, Galipeau J, Gene Ther 2003 10 621 629 10.1038/sj.gt.3301934 12692590 (Pubitemid 36553607)
8. Simvastatin augments the efficacy of therapeutic angiogenesis induced by bone marrow-derived mesenchymal stem cells in a murine model of hindlimb ischemia. Zhang Y, Zhang R, Li Y, He G, Zhang D, Zhang F, Mol Biol Rep 2012 39 285 293 10.1007/s11033-011-0737-y 21553056
9. Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations. Bai K, Huang Y, Jia X, Fan Y, Wang W, J Biomech 2010 43 1176 1181 10.1016/j.jbiomech.2009.11.030 20022602
10. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y, Cell Stem Cell 2008 2 141 150 10.1016/j.stem.2007. 11.014 18371435 (Pubitemid 351181031)
11. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K, Blood 2007 109 228 234 10.1182/blood-2006-02-002246 16985180 (Pubitemid 46053063)
12. Immunomodulatory properties of mesenchymal stromal cells. Nauta AJ, Fibbe WE, Blood 2007 110 3499 3506 10.1182/blood-2007-02-069716 17664353 (Pubitemid 350159613)
13. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Ghannam S, Bouffi C, Djouad F, Jorgensen C, Noel D, Stem Cell Res Ther 2010 1 2 10.1186/scrt2 20504283
14. Transplantation of autologous mononuclear bone marrow stem cells in patients with peripheral arterial disease (the TAM-PAD study). Bartsch T, Brehm M, Zeus T, Kogler G, Wernet P, Strauer BE, Clin Res Cardiol 2007 96 891 899 10.1007/s00392-007-0569-x 17694378 (Pubitemid 350164931)
15. Transendocardial autologous bone marrow mononuclear cell injection in ischemic heart failure: postmortem anatomicopathologic and immunohistochemical findings. Dohmann HF, Perin EC, Takiya CM, Silva GV, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Pascarelli BM, Assis IM, Dutra HS, Assad JA, Castello-Branco RV, Drummond C, Dohmann HJ, Willerson JT, Borojevic R, Circulation 2005 112 521 526 10.1161/CIRCULATIONAHA.104.499178 16027258 (Pubitemid 41060792)
16. Autologous bone-marrow mononuclear cell implantation improves endothelium-dependent vasodilation in patients with limb ischemia. Higashi Y, Kimura M, Hara K, Noma K, Jitsuiki D, Nakagawa K, Oshima T, Chayama K, Sueda T, Goto C, Matsubara H, Murohara T, Yoshizumi M, Circulation 2004 109 1215 1218 10.1161/01.CIR.0000121427.53291.78 15007007 (Pubitemid 38372778)
17. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H, Shimada K, Iwasaka T, Imaizumi T, Therapeutic Angiogenesis using Cell Transplantation (TACT) Study Investigators, Lancet 2002 360 427 435 10.1016/S0140-6736(02)09670-8 12241713
18. Improved exercise capacity and ischemia 6 and 12 months after transendocardial injection of autologous bone marrow mononuclear cells for ischemic cardiomyopathy. Perin EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Silva GV, Mesquita CT, Belém L, Vaughn WK, Rangel FO, Assad JA, Carvalho AC, Branco RV, Rossi MI, Dohmann HJ, Willerson JT, Circulation 2004 110 I213 II218 15364865
19. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T, Proc Natl Acad Sci U S A 2000 97 3422 3427 10.1073/pnas.97.7.3422 10725398 (Pubitemid 30183318)
20. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS, Milliken C, Uchida S, Masuo O, Iwaguro H, Ma H, Hanley A, Silver M, Kearney M, Losordo DW, Isner JM, Asahara T, Circulation 2003 107 461 468 10.1161/01.CIR.0000046450.89986.50 12551872 (Pubitemid 36158050)
21. Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia. Iwase T, Nagaya N, Fujii T, Itoh T, Murakami S, Matsumoto T, Kangawa K, Kitamura S, Cardiovasc Res 2005 66 543 551 10.1016/j.cardiores.2005.02.006 15914119 (Pubitemid 40725766)
22. Bone marrow-derived mesenchymal stem cells from early diffuse systemic sclerosis exhibit a paracrine machinery and stimulate angiogenesis in vitro. Guiducci S, Manetti M, Romano E, Mazzanti B, Ceccarelli C, Dal Pozzo S, Milia AF, Bellando-Randone S, Fiori G, Conforti ML, Saccardi R, Ibba-Manneschi L, Matucci-Cerinic M, Ann Rheum Dis 2011 70 2011 2021 10.1136/ard.2011.150607 21821866
23. Mechanical stress promotes the expression of smooth muscle-like properties in marrow stromal cells. Kobayashi N, Yasu T, Ueba H, Sata M, Hashimoto S, Kuroki M, Saito M, Kawakami M, Exp Hematol 2004 32 1238 1245 10.1016/j.exphem.2004.08.011 15588948 (Pubitemid 39601129)
24. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, Werner C, Stem Cells 2004 22 377 384 10.1634/stemcells.22-3-377 15153614 (Pubitemid 38736621)
25. Therapeutic angiogenesis using autologous bone marrow stromal cells: improved blood flow in a chronic limb ischemia model. Al-Khaldi A, Al-Sabti H, Galipeau J, Lachapelle K, Ann Thorac Surg 2003 75 204 209 10.1016/S0003-4975(02) 04291-1 12537217 (Pubitemid 36099048)
26. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Kinnaird T, Stabile E, Burnett MS, Shou M, Lee CW, Barr S, Fuchs S, Epstein SE, Circulation 2004 109 1543 1549 10.1161/01.CIR.0000124062.31102.57 15023891 (Pubitemid 38420184)
27. Human adipose tissue-derived mesenchymal stem cells improve postnatal neovascularization in a mouse model of hindlimb ischemia. Moon MH, Kim SY, Kim YJ, Kim SJ, Lee JB, Bae YC, Sung SM, Jung JS, Cell Physiol Biochem 2006 17 279 290 10.1159/000094140 16791003 (Pubitemid 43946282)
28. Hypoxia promotes murine bone-marrow-derived stromal cell migration and tube formation. Annabi B, Lee YT, Turcotte S, Naud E, Desrosiers RR, Champagne M, Eliopoulos N, Galipeau J, Beliveau R, Stem Cells 2003 21 337 347 10.1634/stemcells.21-3-337 12743328 (Pubitemid 36623175)
29. Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Silva GV, Litovsky S, Assad JA, Sousa AL, Martin BJ, Vela D, Coulter SC, Lin J, Ober J, Vaughn WK, Branco RV, Oliveira EM, He R, Geng YJ, Willerson JT, Perin EC, Circulation 2005 111 150 156 10.1161/01.CIR.0000151812. 86142.45 15642764 (Pubitemid 40139725)
30. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD, Circulation 2002 105 93 98 10.1161/hc0102.101442 11772882 (Pubitemid 34049148)
31. Mesenchymal stem cells as trophic mediators. Caplan AI, Dennis JE, J Cell Biochem 2006 98 1076 1084 10.1002/jcb.20886 16619257 (Pubitemid 44128350)
32. Umbilical cord-derived mesenchymal stem cells isolated by a novel explantation technique can differentiate into functional endothelial cells and promote revascularization. Xu Y, Meng H, Li C, Hao M, Wang Y, Yu Z, Li Q, Han J, Zhai Q, Qiu L, Stem Cells Dev 2010 19 1511 1522 10.1089/scd.2009.0321 20170363
33. Collateral density, remodeling, and VEGF-A expression differ widely between mouse strains. Chalothorn D, Clayton JA, Zhang H, Pomp D, Faber JE, Physiol Genomics 2007 30 179 191 10.1152/physiolgenomics.00047.2007 17426116 (Pubitemid 47173281)
34. A quantitative trait locus (LSq-1) on mouse chromosome 7 is linked to the absence of tissue loss after surgical hindlimb ischemia. Dokun AO, Keum S, Hazarika S, Li Y, Lamonte GM, Wheeler F, Marchuk DA, Annex BH, Circulation 2008 117 1207 1215 10.1161/CIRCULATIONAHA.107.736447 18285563 (Pubitemid 351544070)
35. Impact of mouse strain differences in innate hindlimb collateral vasculature. Helisch A, Wagner S, Khan N, Drinane M, Wolfram S, Heil M, Ziegelhoeffer T, Brandt U, Pearlman JD, Swartz HM, Schaper W, Arterioscler Thromb Vasc Biol 2006 26 520 526 16397137
36. Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Meirelles Lda S, Nardi NB, Br J Haematol 2003 123 702 711 10.1046/j.1365-2141.2003.04669.x 14616976 (Pubitemid 37468069)
37. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. da Silva ML, Chagastelles PC, Nardi NB, J Cell Sci 2006 119 2204 2213 10.1242/jcs.02932 16684817 (Pubitemid 43960310)
38. Granulocyte-macrophage colony-stimulating factor gene based therapy for acute limb ischemia in a mouse model. Sacramento CB, Cantagalli VD, Grings M, Carvalho LP, Baptista-Silva JC, Beutel A, Bergamaschi CT, de Campos Junior RR, de Moraes JZ, Takiya CM, Samoto VY, Borojevic R, da Silva FH, Nardi NB, Dohmann HF, Junior HS, Valero VB, Han SW, J Gene Med 2009 11 345 353 10.1002/jgm.1298 19194978
39. Treatment of mouse limb ischemia with an integrative hypoxia-responsive vector expressing the vascular endothelial growth factor gene. Yasumura EG, Stilhano RS, Samoto VY, Matsumoto PK, de Carvalho LP, Valero Lapchik VB, Han SW, PLoS One 2012 7 33944 10.1371/journal.pone.0033944 22470498
40. Biological activities encoded by the murine mesenchymal stem cell transcriptome provide a basis for their developmental potential and broad therapeutic efficacy. Phinney DG, Hill K, Michelson C, DuTreil M, Hughes C, Humphries S, Wilkinson R, Baddoo M, Bayly E, Stem Cells 2006 24 186 198 10.1634/stemcells.2004-0236 16100003
41. Autologous bone marrow cell transplantation increases leg perfusion and reduces amputations in patients with advanced critical limb ischemia due to peripheral artery disease. Amann B, Luedemann C, Ratei R, Schmidt-Lucke JA, Cell Transplant 2009 18 371 380 10.3727/096368909788534942 19500466
42. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT, Jayasankar V, Morine KJ, Gardner TJ, Discher DE, Sweeney HL, Am J Physiol Heart Circ Physiol 2006 290 2196 H2203 10.1152/ajpheart.01017.2005 16473959 (Pubitemid 43846045)
43. Successful stem cell therapy using umbilical cord blood-derived multipotent stem cells for Buerger's disease and ischemic limb disease animal model. Kim SW, Han H, Chae GT, Lee SH, Bo S, Yoon JH, Lee YS, Lee KS, Park HK, Kang KS, Stem Cells 2006 24 1620 1626 10.1634/stemcells.2005-0365 16497946 (Pubitemid 44464680)
44. Direct comparison of human mesenchymal stem cells derived from adipose tissues and bone marrow in mediating neovascularization in response to vascular ischemia. Kim Y, Kim H, Cho H, Bae Y, Suh K, Jung J, Cell Physiol Biochem 2007 20 867 876 10.1159/000110447 17982269 (Pubitemid 350059730)
45. Molecular analysis of the differentiation potential of murine mesenchymal stem cells from tissues of endodermal or mesodermal origin. Nora CC, Camassola M, Bellagamba B, Ikuta N, Christoff AP, Meirelles LD, Ayres R, Margis R, Nardi NB, Stem Cells Dev 2012 21 1761 1768 10.1089/scd.2011.0030 21970410
46. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ, Blood 2004 103 1662 1668 10.1182/blood-2003-09-3070 14592819 (Pubitemid 38268957)
47. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T, Arthritis Rheum 2005 52 2521 2529 10.1002/art.21212 16052568 (Pubitemid 41117441)
48. Search for appropriate experimental methods to create stable hind-limb ischemia in mouse. Goto T, Fukuyama N, Aki A, Kanabuchi K, Kimura K, Taira H, Tanaka E, Wakana N, Mori H, Inoue H, Tokai J Exp Clin Med 2006 31 128 132 21302240 (Pubitemid 46785462)
49. Angiogenic gene therapy for experimental critical limb ischemia: acceleration of limb loss by overexpression of vascular endothelial growth factor 165 but not of fibroblast growth factor-2. Masaki I, Yonemitsu Y, Yamashita A, Sata S, Tanii M, Komori K, Nakagawa K, Hou X, Nagai Y, Hasegawa M, Sugimachi K, Sueishi K, Circ Res 2002 90 966 973 10.1161/01.RES.0000019540. 41697.60 12016262 (Pubitemid 34633862)
50. VEGF is critical for stem cell-mediated cardioprotection and a crucial paracrine factor for defining the age threshold in adult and neonatal stem cell function. Markel TA, Wang Y, Herrmann JL, Crisostomo PR, Wang M, Novotny NM, Herring CM, Tan J, Lahm T, Meldrum DR, Am J Physiol Heart Circ Physiol 2008 295 2308 H2314 10.1152/ajpheart.00565.2008 18849336
51. Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia. von Degenfeld G, Banfi A, Springer ML, Wagner RA, Jacobi J, Ozawa CR, Merchant MJ, Cooke JP, Blau HM, FASEB J 2006 20 2657 2659 10.1096/fj.06-6568fje 17095533 (Pubitemid 44953812)
52. Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis. Ozawa CR, Banfi A, Glazer NL, Thurston G, Springer ML, Kraft PE, McDonald DM, Blau HM, J Clin Invest 2004 113 516 527 14966561 (Pubitemid 38542501)
53. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Prockop DJ, Oh JY, Mol Ther 2012 20 14 20 10.1038/mt.2011.211 22008910
54. Human adipose tissue-derived mesenchymal stromal cells as salvage therapy for treatment of severe refractory acute graft-vs.-host disease in two children. Fang B, Song Y, Lin Q, Zhang Y, Cao Y, Zhao RC, Ma Y, Pediatr Transplant 2007 11 814 817 10.1111/j.1399-3046.2007.00780.x 17910665 (Pubitemid 47512333)
55. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, Lanino E, Sundberg B, Bernardo ME, Remberger M, Dini G, Egeler RM, Bacigalupo A, Fibbe W, Ringdén O, Developmental Committee of the European Group for Blood and Marrow Transplantation, Lancet 2008 371 1579 1586 10.1016/S0140-6736(08)60690-X 18468541 (Pubitemid 351626841)
56. Autologous mesenchymal stromal cells and kidney transplantation: a pilot study of safety and clinical feasibility. Perico N, Casiraghi F, Introna M, Gotti E, Todeschini M, Cavinato RA, Capelli C, Rambaldi A, Cassis P, Rizzo P, Cortinovis M, Marasà M, Golay J, Noris M, Remuzzi G, Clin J Am Soc Nephrol 2011 6 412 422 10.2215/CJN.04950610 20930086
57. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG, Proc Natl Acad Sci U S A 2003 100 8407 8411 10.1073/pnas.1432929100 12815096 (Pubitemid 36842558)
58. IFATS collection: fibroblast growth factor-2-induced hepatocyte growth factor secretion by adipose-derived stromal cells inhibits postinjury fibrogenesis through a c-Jun N-terminal kinase-dependent mechanism. Suga H, Eto H, Shigeura T, Inoue K, Aoi N, Kato H, Nishimura S, Manabe I, Gonda K, Yoshimura K, Stem cells 2009 27 238 249 10.1634/stemcells.2008-0261 18772314
59. Evolving paradigms for repair of tissues by adult stem/progenitor cells (MSCs). Prockop DJ, Kota DJ, Bazhanov N, Reger RL, J Cell Mol Med 2010 14 2190 2199 10.1111/j.1582-4934.2010.01151.x 20716123