Heterotopic vascularized murine cardiac transplantation to study graft arteriopathy

Nature Protocols

Volumn 2, Issue 3, 2007, Pages 471-480

  Hasegawa, Tomomi ^a   Visovatti, Scott H ^a   Hyman, Matthew C ^a   Hayasaki, Takanori ^a   Pinsky, David J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND MONOCLONAL ANTIBODY; HLA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OKT 8;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASCENDING AORTA; CARDIAC ALLOGRAFT VASCULOPATHY; CLINICAL FEATURE; CLINICAL PROTOCOL; DIAGNOSTIC PROCEDURE; DONOR; END TO SIDE ANASTOMOSIS; EXPERIMENTAL MODEL; FUNCTIONAL ASSESSMENT; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HEART FAILURE; HEART FUNCTION; HEART TRANSPLANTATION; HEREDITY; HETEROTOPIC TRANSPLANTATION; HISTOCOMPATIBILITY; HLA MATCHING; IMMUNE RESPONSE; INFERIOR CAVA VEIN; MALE; MAMMAL; MEDICAL RESEARCH; MICROSURGERY; MORPHOMETRICS; MOUSE; NONHUMAN; OPERATION DURATION; PRIORITY JOURNAL; PULMONARY ARTERY; RELIABILITY; REPRODUCIBILITY; SURGICAL TECHNIQUE; SUTURING METHOD; VASCULARIZATION; ALLOTRANSPLANTATION; ANIMAL; CORONARY ARTERY DISEASE; DISEASE MODEL; METHODOLOGY; PATHOLOGY;

CHICKEN ANEMIA VIRUS; MAMMALIA; MURINAE;

ANIMALS; CORONARY DISEASE; DISEASE MODELS, ANIMAL; HEART TRANSPLANTATION; MICE; MICROSURGERY; TRANSPLANTATION, HETEROTOPIC; TRANSPLANTATION, HOMOLOGOUS;

EID: 34347237641     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2007.48     Document Type: Article

References (73)

1. Steinman, T.I. et al. Guidelines for the referral and management of patients eligible for solid organ transplantation. Transplantation 71, 1189-1204 (2001).
2. Orens, J.B. et al. Thoracic organ transplantation in the United States, 1995-2004. Am. J. Transplant. 6, 1188-1197 (2006).
3. Taylor, D.O. et al. Registry of the International Society for Heart and Lung Transplantation: Twenty-third official adult heart transplantation report - 2006. J. Heart Lung Transplant. 25, 869-879 (2006).
4. Gao, S.Z. et al. Acute myocardial infarction in cardiac transplant recipients. Am. J. Cardiol. 64, 1093-1097 (1989).
5. Stoica, S.C., Goddard, M. & Large, S.R. The endothelium in clinical cardiac transplantation. Ann. Thorac. Surg. 73, 1002-1008 (2002).
6. Uehara, S. et al. NK cells can trigger allograft vasculopathy: The role of hybrid resistance in solid organ allografts. J. Immunol. 175, 3424-3430 (2005).
7. Billingham, M.E. Histopathology of graft coronary disease. J. Heart Lung Transplant. 11, S38-S44 (1992).
8. Weis, M. & von Scheidt, W. Coronary artery disease in the transplanted heart. Annu. Rev. Med. 51, 81-100 (2000).
9. Barnard, C.N. The operation. A human cardiac transplant: An interim report of a successful operation performed at Groote Schuur Hospital, Cape Town. S. Afr. Med. J. 41, 1271-1274 (1967).
10. Kadner, A., Chen, R.H. & Adams, D.H. Heterotopic heart transplantation: experimental development and clinical experience. Eur. J. Cardiothorac. Surg. 17, 474-481 (2000).
11. Carrel, A. & Guthrie, C.C. The transplantation of veins and organs. Am. Med. 10, 1101-1102 (1905).
12. Mann, F.C., Priestley, J.T., Markowitz, J. & Yater, W.M. Transplantation of the intact mammalian heart. Arch. Surg. 26, 219-224 (1933).
13. Chiba, C. et al. Studies on the transplanted heart. Its metabolism and histology. J. Exp. Med. 115, 853-866 (1962).
14. Heron, I. A technique for accessory cervical heart transplantation in rabbits and rats. Acta Pathol. Microbiol. Scand. [A] 79, 366-372 (1971).
15. Marcus, E., Wong, S.N. & Luisada, A.A. Homologous heart grafts. I. Technique of interim parabiotic perfusion. II. Transplantation of the heart in dogs. AMA Arch. Surg. 66, 179-191 (1953).
16. Neptune, W.B., Cookson, B.A., Bailey, C.P., Appler, R. & Rajkowski, F. Complete homologous heart transplantation. AMA Arch. Surg. 66 174-178 (1953).
17. Sayegh, S.F., Creech, O. Jr. & Harding, J.H. Transplantation of the homologous heart. Surg. Forum 8, 317-319 (1957).
18. Fulmer, R.I., Cramer, A.T., Liebelt, R.A. & Liebelt, A.G. Transplantation of cardiac tissue into the mouse ear. Am. J. Anat. 113, 273-285 (1963).
19. Judd, K.P. & Trentin, J.J. Cardiac transplantation in mice. I. Factors influencing the take and survival of heterotopic grafts. Transplantation 11, 298-302 (1971).
20. Giardina, J.J. et al. Use of cyclosporine in the mouse heterotopic heart transplant model. J. Heart Transplant. 9, 106-113 (1990).
21. Koehl, G.E. et al. Rapamycin protects allografts from rejection while simultaneously attacking tumors in immunosuppressed mice. Transplantation 77, 1319-1326 (2004).
22. Mazer, S.P. & Pinsky, D.J. Alive and kicking: Endothelium at the geographic nexus of vascular rejection. Circ. Res. 91, 1085-1088 (2002).
23. Abbott, C.P., Lindsey, E.S., Creech, O. Jr. & Dewitt, C.W. A technique for heart transplantation in the rat. Arch. Surg. 89, 645-652 (1964).
24. Ono, K. & Lindsey, E.S. Improved technique of heart transplantation in rats. J. Thorac. Cardiovasc. Surg. 57, 225-229 (1969).
25. Corry, R.J., Winn, H.J. & Russell, P.S. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 16, 343-350 (1973).
26. Asfour, B. et al. A simple new model of physiologically working heterotopic rat heart transplantation provides hemodynamic performance equivalent to that of an orthotopic heart. J. Heart Lung Transplant. 18, 927-936 (1999).
27. Chen, Z.H. A technique of cervical heterotopic heart transplantation in mice. Transplantation 52, 1099-1101 (1991).
28. Matsuura, A., Abe, T. & Yasuura, K. Simplified mouse cervical heart transplantation using a cuff technique. Transplantation 51, 896-898 (1991).
29. Tomita, Y. et al. Improved technique of heterotopic cervical heart transplantation in mice. Transplantation 64, 1598-1601 (1997).
30. Niimi, M. The technique for heterotopic cardiac transplantation in mice: experience of 3000 operations by one surgeon. J. Heart Lung Transplant. 20, 1123-1128 (2001).
31. Iwanaga, K. et al. Riboflavin-mediated reduction of oxidant injury, rejection, and vasculopathy following cardiac allotransplantation. Transplantation (in press).
32. Medawar, P.B. The behavior and fate of skin autografts and skin homografts in rabbits. J. Anat. 78, 176-179 (1944).
33. (-/-) mice show the importance of major histocompatibility complex-bound peptide in cardiac allograft rejection. J. Exp. Med. 192, 31-40 (2000).
34. George, J.F., Pinderski, L.J., Litovsky, S. & Kirklin, J.K. Of mice and men: Mouse models and the molecular mechanisms of post-transplant coronary artery disease. J. Heart Lung Transplant. 24, 2003-2014 (2005).
35. Eichwald, E.J., Silmser, C.R. & Weissman, I. Sex-linked rejection of normal and neoplastic tissue. I. Distribution and specificity. J. Natl. Cancer Inst. 20, 563-575 (1958).
36. Bailey, D.W. Allelic forms of a gene controlling the female immune response to the male antigen in mice. Transplantation 11, 426-428 (1971).
37. Bailey, D.W. & Hoste, J. A gene governing the female immune response to the male antigen in mice. Transplantation 11, 404-407 (1971).
38. Furukawa, Y., Mandelbrot, D.A., Libby, P., Sharpe, A.H. & Mitchell, R.N. Association of B7-1 co-stimulation with the development of graft arterial disease. Studies using mice lacking B7-1, B7-2, or B7-1/B7-2. Am. J. Pathol. 157, 473-484 (2000).
39. Russell, P.S., Chase, C.M., Winn, H.J. & Colvin, R.B. Coronary atherosclerosis in transplanted mouse hearts. I. Time course and immunogenetic and immunopathological considerations. Am. J. Pathol. 144, 260-274 (1994).
40. Pinsky, D. et al. Restoration of the cAMP second messenger pathway enhances cardiac preservation for transplantation in a heterotopic rat model. J. Clin. Invest. 92, 2994-3002 (1993).
41. Wang, C.Y. et al. cAMP pulse during preservation inhibits the late development of cardiac isograft and allograft vasculopathy. Circ.Res. 86, 982-988 (2000).
42. Billingham, M.E. et al. A working formulation for the standardization of nomenclature in the diagnosis of heart and lung rejection: Heart Rejection Study Group. The International Society for Heart Transplantation. J. Heart Transplant. 9, 587-593 (1990).
43. Stewart, S. et al. Revision of the 1990 working formulation for the standardization of nomenclature in the diagnosis of heart rejection. J. Heart Lung Transplant. 24, 1710-1720 (2005).
44. + T lymphocytes prevents the development of cardiac allograft vasculopathy. Transplantation 73, 1116-1122 (2002).
45. Schnickel, G.T. et al. CD8 lymphocytes are sufficient for the development of chronic rejection. Transplantation 78, 1634-1639 (2004).
46. Glysing-Jensen, T., Raisanen-Sokolowski, A., Sayegh, M.H. & Russell, M.E. Chronic blockade of CD28-B7-mediated T-cell costimulation by CTLA4Ig reduces intimal thickening in MHC class I and II incompatible mouse heart allografts. Transplantation 64, 1641-1645 (1997).
47. Larsen, C.P. et al. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 381 434-438 (1996).
48. Wang, C.Y. et al. Suppression of murine cardiac allograft arteriopathy by long-term blockade of CD40-CD154 interactions. Circulation 105, 1609-1614 (2002).
49. + T cellmediated alloimmune responses in vivo. J. Immunol. 174, 1357-1364 (2005).
50. Zand, M.S. et al. Interleukin-2 and interferon-gamma double knockout mice reject heterotopic cardiac allografts. Transplantation 70, 1378-1381 (2000).
51. Fischbein, M.P. et al. Regulated interleukin-10 expression prevents chronic rejection of transplanted hearts. J. Thorac. Cardiovasc. Surg. 126, 216-223 (2003).
52. Nagano, H. et al. Interferon-gamma deficiency prevents coronary arteriosclerosis but not myocardial rejection in transplanted mouse hearts. J. Clin. Invest. 100, 550-557 (1997).
53. McKee, C.M. et al. Prolonged allograft survival in TNF receptor 1-deficient recipients is due to immunoregulatory effects, not to inhibition of direct antigraft cytotoxicity. J. Immunol. 168 483-489 (2002).
54. Dietrich, H. et al. Mouse model of transplant arteriosclerosis: role of intercellular adhesion molecule-1. Arterioscler. Thromb. Vasc. Biol. 20, 343-352 (2000).
55. Ardehali, A., Laks, H., Drinkwater, D.C., Ziv, E. & Drake, T.A. Vascular cell adhesion molecule-1 is induced on vascular endothelia and medial smooth muscle cells in experimental cardiac allograft vasculopathy. Circulation 92, 450-456 (1995).
56. Wang, C.Y. et al. Cardiac graft intercellular adhesion molecule-1 (ICAM-1) and interleukin-1 expression mediate primary isograft failure and induction of ICAM-1 in organs remote from the site of transplantation. Circ. Res. 82, 762-772 (1998).
57. Russell, P.S., Chase, C.M. & Colvin, R.B. Coronary atherosclerosis in transplanted mouse hearts. IV effects of treatment with monoclonal antibodies to intercellular adhesion molecule-1 and leukocyte function-associated antigen-1. Transplantation 60, 724-729 (1995).
58. Densem, C.G., Hutchinson, I.V., Cooper, A., Yonan, N. & Brooks, N.H. Polymorphism of the transforming growth factor-beta 1 gene correlates with the development of coronary vasculopathy following cardiac transplantation. J. Heart Lung. Transplant. 19, 551-556 (2000).
59. Mancini, M.C. & Evans, J.T. Role of platelet-derived growth factor in allograft vasculopathy. Ann. Surg. 231, 682-688 (2000).
60. Csencsits, K. et al. Transforming growth factor beta-induced connective tissue growth factor and chronic allograft rejection. Am. J. Transplant. 6, 959-966 (2006).
61. Akashi, S. et al. A novel small-molecule compound targeting CCR5 and CXCR3 prevents acute and chronic allograft rejection. Transplantation 80, 378-384 (2005).
62. Yun, J.J. et al. Combined blockade of the chemokine receptors CCR1 and CCR5 attenuates chronic rejection. Circulation 109, 932-937 (2004).
63. Okada, M. et al. Transcriptional control of cardiac allograft vasculopathy by early growth response gene-1 (Egr-1). Circ. Res. 91, 135-142 (2002).
64. Suzuki, J. et al. Prevention of graft coronary arteriosclerosis by antisense cdk2 kinase oligonucleotide. Nat. Med. 3, 900-903 (1997).
65. Koglin, J., Glysing-Jensen, T., Gadiraju, S. & Russell, M.E. Attenuated cardiac allograft vasculopathy in mice with targeted deletion of the transcription factor STAT4. Circulation 101, 1034-1039 (2000).
66. Yamashita, K. et al. Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J. 20, 776-778 (2006).
67. Weis, M. & Cooke, J.P. Cardiac allograft vasculopathy and dysregulation of the NO synthase pathway. Arterioscler. Thromb. Vasc. Biol. 23, 567-575 (2003).
68. Russell, P.S., Chase, C.M. & Colvin, R.B. Accelerated atheromatous lesions in mouse hearts transplanted to apolipoprotein-E-deficient recipients. Am. J. Pathol. 149, 91-99 (1996).
69. Tanaka, M. et al. In vivo visualization of cardiac allograft rejection and trafficking passenger leukocytes using bioluminescence imaging. Circulation 112, I105-I110 (2005).
70. Tanaka, M. et al. Dimethylarginine dimethylaminohydrolase overexpression suppresses graft coronary artery disease. Circulation 112, 1549-1556 (2005).
71. Tanaka, M. et al. Overexpression of human copper/zinc superoxide dismutase (SOD1) suppresses ischemia-reperfusion injury and subsequent development of graft coronary artery disease in murine cardiac grafts. Circulation 110, II200-II206 (2004).
72. Janssen, B.J. et al. Effects of anesthetics on systemic hemodynamics in mice. Am. J. Physiol. Heart Circ. Physiol. 287 H1618-H1624 (2004).
73. Kawahara, Y. et al. Preferable anesthetic conditions for echocardiographic determination of murine cardiac function. J. Pharmacol. Sci. 99, 95-104 (2005).