Ferritin as a reporter gene for in vivo tracking of stem cells by 1.5-T cardiac MRI in a rat model of myocardial infarction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 300, Issue 6, 2011, Pages

  Campan, Manuela ^a   Lionetti, Vincenzo ^a,b   Aquaro, Giovanni D ^b   Forini, Francesca ^b   Matteucci, Marco ^a   Vannucci, Laura ^c   Chiuppesi, Flavia ^c   di Cristofano, Claudio ^e   Faggioni, Michela ^a   Maioli, Margherita ^d   Barile, Lucio ^f   Messina, Elisa ^g   Lombardi, Massimo ^b   Pucci, Angela ^h   Pistello, Mauro ^c   Recchia, Fabio A ^a,i  

^a SCUOLA SUPERIORE SANT ANNA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF PISA   (Italy)

^d UNIVERSITY OF SASSARI   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f UNIVERSITY OF MILANO BICOCCA   (Italy)

^g SAPIENZA UNIVERSITY OF ROME   (Italy)

^h UNIVERSITY HOSPITAL OF PISA   (Italy)

ⁱ NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Cell tracking; Magnetic resonance imaging

Indexed keywords

ALPHA SARCOMERIC ACTIN ANTIGEN; ALPHA SMOOTH MUSCLE ACTIN; ANTIGEN; CD31 ANTIGEN; FERRITIN; HUMAN FERRITIN HEAVY CHAIN; LENTIVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL TRACKING; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE; HISTOPATHOLOGY; HUMAN; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MORPHOLOGY; NICK END LABELING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; REPORTER GENE; SMOOTH MUSCLE FIBER; STEM CELL; SWINE;

ACTINS; ANIMALS; ANTIGENS, CD31; APOFERRITINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; GENES, REPORTER; HUMANS; LENTIVIRUS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, ANIMAL; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; RATS, WISTAR; STEM CELL TRANSPLANTATION; STEM CELLS; SWINE; TRANSDUCTION, GENETIC;

EID: 79957598517     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00935.2010     Document Type: Article

References (56)

1. 2+ signaling as an index of cardiac progenitor cells differentiation. Basic Res Cardiol 105: 737-749, 2010.
2. Amsalem Y, Mardor Y, Feinberg MS, Landa N, Miller L, Daniels D, Ocherashvilli A, Holbova R, Yosef O, Barbash IM, Leor. Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation 116: I38-I45, 2007.
3. Anderson LJ, Holden S, Davis B, Prescott E, Charrier CC, Bunce NH, Firmin DN, Wonke B, Porter J, Walker JM, Pennell DJ. Cardiovascular T2-star (T2) magnetic resonance for the early diagnosis of myocardial iron overload. Eur Heart J 22: 2171-2179, 2001.
4. Aung W, Hasegawa S, Koshikawa-Yano M, Obata T, Ikehira H, Furukawa T, Aoki I, Saga T. Visualization of in vivo electroporationmediated transgene expression in experimental tumors by optical and magnetic resonance imaging. Gene Ther 16: 830-839, 2009.
5. Bohle RM, Pich S, Klein HH. Modulation of the inflammatory response in experimental myocardial infarction. Eur Heart J 12 Suppl D: 28-31, 1991.
6. Cao F, Lin S, Xie X, Ray P, Patel M, Zhang X, Drukker M, Dylla SJ, Connolly AJ, Chen X, Weissman IL, Gambhir SS, Wu JC. In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 113: 1005-1014, 2006.
7. Cheng K, Li TS, Malliaras K, Davis DR, Zhang Y, Marban E. Magnetic targeting enhances engraftment and functional benefit of ironlabeled cardiosphere-derived cells in myocardial infarction. Circ Res 106: 1570-1581, 2010.
8. Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A, Marba'n E. Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infracted mice. Circ Res 106: 971-980, 2010.
9. Choi-Hong SR, Genest DR, Crum CP, Berkowits R, Goldstein DP, Schofield DE. Twin pregnancies with complete hydatidiform mole and coexisting fetus: use of fluorescent in situ hybridization to evaluate placental X- and Y-chromosomal content. Hum Pathol 26: 1175-1180, 1995.
10. Cohen B, Dafni H, Meir G, Harmeliny A, Neeman M. Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia 7: 109-117, 2005.
11. Cozzi A, Corsi B, Levi S, Santambrogio P, Albertini A, Arosio P. Overexpression of wild type and mutated human ferritin H-chain in HeLa cells: in vivo role of ferritin ferroxidase activity. J Biol Chem 275: 25122-25129, 2000.
12. Dai W, Hale SL, Martin BJ, Kuang JQ, Dow JS, Wold LE, Kloner RA. Allogeneic mesenchymal stem cell transplantation in postinfarcted rat myocardium: short-and long-term effects. Circulation 112: 214-223, 2005.
13. Deans AE, Wadghiri YZ, Bernas LM, Yu X, Rutt BK, Turnbull DH. Cellular MRI contrast via coexpression of transferrin receptor and ferritin. Magn Reson Med 56: 51-59, 2006.
14. Segura MM, Kamen A, Garnier A. Downstream processing of oncoretroviral and lentiviral gene therapy vectors. Biotechnol Adv 24: 321-337, 2006.
15. Forini F, Lionetti V, Ardehali H, Pucci A, Cecchetti F, Ghanefar M, Nicolini G, Ichikawa Y, Nannipieri M, Recchia FA, Iervasi G. Early long-term L-T3 replacement rescues mitochondria and prevents ischemic cardiac remodeling in rats. J Cell Mol Med. In press.
16. Garot J, Unterseeh T, Teiger E, Champagne S, Chazaud B, Gherardi R, Hittinger L, Guéret P, Rahmouni A. Magnetic resonance imaging of targeted catheter-based implantation of myogenic precursor cells into infarcted left ventricular myocardium. J Am Coll Cardiol 41: 1841-1846, 2003.
17. Genove G, DeMarco U, Xu H, Goins WF, Ahrens ET. A new transgene reporter for in vivo magnetic resonance imaging. Nat Med 11: 450-454, 2005.
18. Gilson WD, Kraitchman DL. Cardiac magnetic resonance imaging in small rodents using clinical 1.5T and 30T scanners. Methods 43: 35-45, 2007.
19. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 103: 1204-1219, 2008.
20. Grenier G, Scimè A, Le Grand F, Asakura A, Perez-Iratxeta C, Andrade-Navarro MA, Labosky PA, Rudnicki MA. Resident endothelial precursors in muscle, adipose, and dermis contribute to postnatal vasculogenesis. Stem Cells 25: 3101-3110, 2007.
21. Gude N, Muraski J, Rubio M, Kajstura J, Schaefer E, Anversa P, Sussman MA. Akt promotes increased cardiomyocyte cycling and expansion of the cardiac progenitor cell population. Circ Res 99: 381-388, 2006.
22. Gyöngyösi M, Blanco J, Marian T, Trón L, Petneházy O, Petrasi Z, Hemetsberger R, Rodriguez J, Font G, Pavo IJ, Kertész I, Balkay L, Pavo N, Posa A, Emri M, Galuska L, Kraitchman DL, Wojta J, Huber K, Glogar D. Serial noninvasive in vivo positron emission tomographic tracking of percutaneously intramyocardially injected autologous porcine mesenchymal stem cells modified for transgene reporter gene expression. Circ Cardiovasc Imaging 1: 94-103, 2008.
23. Hill JM, Dick AJ, Raman VK, Thompson RB, Yu ZX, Hinds KA, Pessanha BS, Guttman MA, Varney TR, Martin BJ, Dunbar CE, McVeigh ER, Lederman RJ. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 108: 1009-1014, 2003.
24. Ju S, Teng G, Zhang Y, Ma M, Chen F, Ni Y. In vitro labeling and MRI of mesenchymal stem cells from human umbilical cord blood. Magn Reson Imaging 24: 611-617, 2006.
25. Kim YJ, Huh YM, Choe KO, Choi BW, Choi EJ, Jang Y, Lee JM, Suh JS. In vivo magnetic resonance imaging of injected mesenchymal stem cells in rat myocardial infarction; simultaneous cell tracking and left ventricular function measurement. Int J Cardiovasc Imaging Suppl 1: 99-109, 2009.
26. Kraitchman DL, Bulte JWM. Imaging of stem cells using MRI. Basic Res Cardiol 103: 105-113, 2008.
27. Kraitchman DL, Heldman AW, Atalar E, Amado LC, Martin BJ, Pittenger MF, Hare JM, Bulte JW. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 107: 2290-2293, 2003.
28. Küstermann E, Roell W, Breitbach M, Wecker S, Wiedermann D, Buehrle C, Welz A, Hescheler J, Fleischmann BK, Hoehn M. Stem cell implantation in ischemic mouse heart: a high-resolution magnetic resonance imaging investigation. NMR Biomed 18: 362-370, 2005.
29. Lewis Carl SA, Gillete-Ferguson I, Ferguson DG. An indirect immunofluorescence procedure for staining the same cryosection with two mouse monoclonal primary antibodies. J Histochem Cytochem 41: 1273-1278, 1993.
30. Lionetti V, Cantoni S, Cavallini C, Bianchi F, Valente S, Frascari I, Olivi E, Aquaro GD, Bonavita F, Scarlata I, Maioli M, Vaccari V, Tassinari R, Bartoli A, Recchia FA, Pasquinelli G, Ventura C. Hyaluronan mixed esters of butyric and retinoic acid affording myocardial survival and repair without stem cell transplantation. J Biol Chem 285: 9949-9961, 2010.
31. Liu J, Cheng EC, Long RC Jr, Yang SH, Wang L, Cheng PH, Yang JJ, Wu D, Mao H, Chan AW. Noninvasive monitoring of embryonic stem cells in vivo with MRI transgene reporter. Tissue Eng Part C Methods 15: 739-747, 2009.
32. Messina E, De Angelis L, Frati G, Morrone S, Chimenti S, Fiordaliso F, Salio M, Battaglia M, Latronico MV, Coletta M, Vivarelli E, Frati L, Cossu G, Giacomello A. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95: 911-921, 2004.
33. Michelini M, Papini S, Rosellini A, Noia G, Ligato MS, Mancuso S, Cavazzana A, Bertacca G, Di Cristofano C, Saccardi R, Urbani S, Revoltella RP. Prolonged human/sheep cellular chimerism following transplantation of human hemopoietic stem cells into the ewe celomic cavity. Int J Dev Biol 52: 365-370, 2008.
34. Müller-Ehmsen J, Krausgrill B, Burst V, Schenk K, Neisen UC, Fries JW, Fleischmann BK, Hescheler J, Schwinger RH. Effective engraftment but poor mid-term persistence of mononuclear and mesenchymal bone marrow cells in acute and chronic rat myocardial infarction. J Mol Cell Cardiol 41: 876-884, 2006.
35. Olivetti G, Ricci R, Beghi C, Guideri G, Anversa P. Response of the border zone to myocardial infarction in rats. Am J Pathol 125: 476-483, 1986.
36. Ono K, Fuma K, Tabata K, Sawada M. Ferritin reporter used for gene expression imaging by magnetic resonance. Biochem Biophys Res Commun 388: 589-594, 2009.
37. Parish CR. Fluorescent dyes for lymphocyte migration and proliferation studies. Immunol Cell Biol 77: 499-508, 1999.
38. Pepe A, Lombardi M, Positano V, Cracolici E, Capra M, Malizia R, Prossomariti L, De Marchi D, Midiri M, Maggio A. Evaluation of the efficacy of oral deferiprone in beta-thalasemia major by multislice multiecho T2. Eur J Haematol 76: 183-92, 2006.
39. Pepe A, Lombardi M, Positano V, Cracolici E, Capra M, Malizia R, Prossomariti L, De Marchi D, Midiri M, Maggio A. Multislice multiecho T2 cardiovascular magnetic resonance for detection of the heterogeneous distribution of myocardial iron overload. J Magn Reson Imaging 23: 662-668, 2006.
40. Pistello M, Bonci F, Flynn JN, Mazzetti P, Isola P, Zabogli E, Camerini V, Matteucci D, Freer G, Pelosi P, Bendinelli M. AIDS vaccination studies with an ex vivo feline immunodeficiency virus model: analysis of the accessory ORF-A protein and DNA as protective immunogens. J Virol 80: 8856-8868, 2006.
41. Pistello M, Vannucci L, Ravani A, Bonci F, Chiuppesi F, Del Santo B, Freer G, Bendinelli M. Streamlined design of a self-inactivating feline immunodeficiency virus vector for transducing ex vivo dendritic cells and T lymphocytes. Genet Vaccines Ther 5: 8, 2007.
42. Potapova IA, Doronin SV, Kelly DJ, Rosen AB, Schuldt AJ, Lu Z, Kochupura PV, Robinson RB, Rosen MR, Brink PR, Gaudette GR, Cohen IS. Enhanced recovery of mechanical function in the canine heart by seeding an extracellular matrix patch with mesenchymal stem cells committed to a cardiac lineage. Am J Physiol Heart Circ Physiol 295: H2257-H2263, 2008.
43. Ramazzotti A, Pepe A, Positano V, Rossi G, De Marchi D, Brizi MG, Luciani A, Midiri M, Sallustio G, Valeri G, Caruso V, Centra M, Cianciulli P, De Sanctis V, Maggio A, Lombardi M. Multicenter validation of the magnetic resonance T2 technique for segmental and global quantification of myocardial iron. J Magn Reson Imaging 30: 62-68, 2009.
44. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marbán E. Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115: 896-908, 2007.
45. Summersgill BM, Shipley JM. Fluorescence in situ hybridization analysis of formalin fixed paraffin embedded tissues, including tissue microarrays. Methods Mol Biol 659: 51-70, 2010.
46. Sun S, Arosio P, Levi S, Chasteen ND. Ferroxidase kinetics of human liver apoferritin, recombinant H-chain apoferritin, and site-directed mutants. Biochemistry 32: 9362-9369, 1993.
47. Tao-Sheng L, Lee ST, Matsushita S, Davis D, Zhang Y, Smith RR, Marban Davis E. Molecular, cellular, and functional phenotypes of human cardiac stem cells dependent upon monolayer versus three-dimensional culture conditions (Abstract). Circ Res 105: e55-e62, 2009.
48. Terrovitis J, Stuber M, Youssef A, Preece S, Leppo M, Kizana E, Schär M, Gerstenblith G, Weiss RG, Marbán E, Abraham MR. Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation 117: 1555-1562, 2008.
49. Tham E, Wang J, Piehl F, Weber G. Upregulation of VEGF-A without angiogenesis in a mouse model of dilated cardiomyopathy caused by mitochondrial dysfunction. J Histochem Cytochem 50: 935-944, 2002.
50. Theophile K, Jonigk D, Kreipe H, Bock O. Amplification of mRNA from laser-microdissected single or clustered cells in formalin-fixed and paraffin-embedded tissues for application in quantitative real-time PCR. Diagn Mol Pathol 17: 101-106, 2008.
51. van Tuyn J, Atsma DE, Winter EM, van der Velde-van Dijke I, Pijnappels DA, Bax NA, Knaän-Shanzer S, Gittenberger-de Groot AC, Poelmann RE, van der Laarse A, van der Wall EE, Schalij MJ, de Vries AA. Epicardial cells of human adults can undergo an epithelialto- mesenchymal transition, and obtain characteristics of smooth muscle cells in vitro. Stem Cells 25: 271-278, 2007.
52. Ventura C, Cantoni S, Bianchi F, Lionetti V, Cavallini C, Scarlata I, Foroni L, Maioli M, Bonsi L, Alviano F, Fossati V, Bagnara GP, Pasquinelli G, Recchia FA, Perbellini A. Hyaluronan mixed esters of butyric and retinoic Acid drive cardiac and endothelial fate in term placenta human mesenchymal stem cells and enhance cardiac repair in infarcted rat hearts. J Biol Chem 282: 14243-14252, 2007.
53. Westwood M, Anderson LJ, Firmin DN, Gatehouse PD, Charrier CC, Wonke B, Pennell DJ. A single breath-hold multiecho T2 cardiovascular magnetic resonance technique for diagnosis of myocardial iron overload. J Magn Reson Imaging 18: 33-39, 2003.
54. Willmann JK, Paulmurugan R, Rodriguez-Porcel M, Stein W, Brinton TJ, Connolly AJ, Nielsen CH, Lutz AM, Lyons J, Ikeno F, Suzuki Y, Rosenberg J, Chen IY, Wu JC, Yeung AC, Yock P, Robbins RC, Gambhir SS. Imaging gene expression in human mesenchymal stem cells: from small to large animals. Radiology 252: 117-127, 2009.
55. Ye L, Haider HKh Jiang S, Tan RS, Ge R, Law PK, Sim EK. Improved angiogenic response in pig heart following ischaemic injury using human skeletal myoblast simultaneously expressing VEGF165 and angiopoietin- 1. Eur J Heart Fail 9: 15-22, 2007.
56. Ziv K, Meir G, Harmelin A, Shimoni E, Klein E, Neeman M. Ferritin as a reporter gene for MRI: chronic liver over expression of h-ferritin during dietary iron supplementation and aging. NMR Biomed 23: 523-531, 2010.