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Organ xenografting between rodents: an evolutionary perspective

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Transplant International

Abstract

Rejection times of heart xenografts in several donor-recipient combinations including the guinea pig, rat, hamster, and mouse are examined in light of the paleontological history of rodents and the resulting phylogenetic distances between taxa. This multidisciplinary review at the molecular, chromosomal and morphological levels suggests that xenograft rejection time is inversely proportional to the time divergence or phylogenetic distance, and that the binomial terminology concordant/discordant does not reflect the amplitude of phylogenetic distances.

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References

  1. Adachi H, Rosengard BR, Hutchins GM, Hall TS, Baumgartner WA, Borkon AM, Reitz BA (1987) Effect of cyclosporine, aspirin, and cobra venom factor on discordant cardiac xenograft survival in rats. Transplant Proc 19: 1145–1148

    Google Scholar 

  2. Aksentijevitch I, Sharabi Y, Sundt TM, Sachs DH, Sykes M (1991) Humoral tolerance in mixed xenogeneic chimeras prepared by a non myelo ablative conditioning regimen. Transplant Proc 23: 880–882

    Google Scholar 

  3. Allard M, Miyamoto MM, Honeycutt RL (1991) Are rodents polyphyletic? Nature 353: 649–650

    Google Scholar 

  4. Auchincloss H Jr (1988) Xenogeneic transplantation. Transplantation 46: 1–20

    Google Scholar 

  5. Beintema JJ (1985) Amino acid sequence data and evolutionary relationships among hystricognaths and other rodents. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 549–565

    Google Scholar 

  6. Bogaerde J van den, White D, Roser B, Kampinga J, Aspinall R (1990) In vitro and in vivo effects of monoclonal antivodies against T cell subsets on allogeneic and xenogeneic responses in the rat. Transplantation 50: 515–522

    Google Scholar 

  7. Bonhomme F, Iskandar D, Thaler L, Petter F (1985) Electromorphs and phylogeny in muroid rodents. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 671–683

    Google Scholar 

  8. Bugge J (1985) Systematic value of the carotid arterial pattern. In: Luckett WP Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 355–379

    Google Scholar 

  9. Burdick JF, Jooste SV, Winn HJ (1979) Variations in the responses of mouse strains to rat xenografts. J Immunol 123: 954–957

    Google Scholar 

  10. Burdick JF, Russel PS, Winn HJ (1979) Sensibility of long-standing xenografts of rat hearts to humoral antibodies. J Immunol 123: 1732–1735

    Google Scholar 

  11. Calne RY (1970) Organ transplantation between widely disparate species. Transplant Proc 2: 550–552

    Google Scholar 

  12. Carleton MD, Musser GG (1984) Muroid rodents. In: Anderson S, Jones JK (eds) Orders and families of recent mammals of the world. Wiley, New York, 289–379

    Google Scholar 

  13. Carroll RL (1988) Vertebrate paleontology and evolution. WH Freeman and Co, New York

    Google Scholar 

  14. Cattel V, Jamieson SW (1975) Hyperacute rejection of guinea pig to rat cardiac xenografts. I. Morphology. J Pathol 115: 183–187

    Google Scholar 

  15. Catzeflis F, Jaeger JJ (1992) Muroid rodents phylogeny and evolution. Trends Ecol Evol 7: 122–133

    Google Scholar 

  16. Chaline J, Graf JD (1986) Phylogeny of the arvicolidae (rodential): biochemical and paleontological evidences. J Mamm 69: 22–33

    Google Scholar 

  17. Chaline J, Mein P (1979) Les rongeurs et l'evolution. Doin, Paris

    Google Scholar 

  18. Chaline J, Mein P, Petter F (1977) Les grandes lignes d'une classification évolutive des Muroidea. Mammalia 41: 245–252

    Google Scholar 

  19. Chavez-Peon F, Monchik F, Winn HJ, Russel PS (1971) Humoral factors in experimental renal allograft and xenograft rejection. Transplant Proc 3: 573–576

    Google Scholar 

  20. Devillers C, Chaline J (1993) Evolution, an evolving theory. Springer Verlag, Heidelberg

    Google Scholar 

  21. Ellerman JR (1940) The families and genera of living rodents. British Mus Nat Hist, London

    Google Scholar 

  22. Flynn LJ, Jacobs LL, Lindsay EH (1985) Problems in muroid phylogeny: relationship to other rodents and origin of major group. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 589–616

    Google Scholar 

  23. Flynn LJ, Jacobs LL, Cheema IU (1986) Baluchimyinae, a new ctenodactyloid rodent subfamily from the Miocene of Beluchistan. Am Mus Novit 2841: 1–58

    Google Scholar 

  24. Gambiez L, Salame E, Chereau C, Calmus Y, Ayani E, Houssin D, Weill B (1992) Natural IgM play a major role in hyperacute rejection of discordant heart xenografts. Transplant Proc 24: 441–442

    Google Scholar 

  25. George W (1985) Reproductive and chromosomal characters of ctenodactylids as a key to their evolutionary relationships. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 453–474

    Google Scholar 

  26. Grassé PP, Dekeyser PL (1955) Ordre des rongeurs. In: Grassé PP (ed) Traité de zoologie. Masson, Paris pp 1321–1525

    Google Scholar 

  27. Graur D, Winston AH, Li WH (1991) Is the guinea pig a rodent? Nature 351: 649–651

    Google Scholar 

  28. Hardy MA, Oluwole S, Fawwaz R, Satake K, Nowygrod R, Reemtsma K (1992) Selective lymphoid iradiation. III. Prolongation of cardiac xenografts and allografts in presensitized rats. Transplantation 33: 237–243

    Google Scholar 

  29. Hartenberger JL (1985) The order rodentia: major questions on their evolutionary origin, relationships and suprafamilial systematics. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 1–33

    Google Scholar 

  30. Homan WP, Williams KA, Fabre JW, Millard PR, Morris PJ (1981) Prolongation of cardiac xenograft survival in rats receiving cyclosporin A. Transplantation 31: 164–166

    Google Scholar 

  31. Houssin D, Bellon B, Brunaud MD, Gugenheim J, Settaf A, Meriggi F, Emond J (1986) Interactions between liver allografts and lymphocytotoxic alloantibodies in inbred rats. Hepatology 6: 994–998

    Google Scholar 

  32. Jaeger JJ (1988) Rodent phylogeny: new data and old problems. In: Benton MJ (ed) The phylogeny and classification of tetrapods. Systematic Assoc 35B: 177–198

  33. Jamieson SW (1974) Xenograft hyperacute rejection: a new model. Transplantation 17: 533–534

    Google Scholar 

  34. Jong WW de (1985) Superordinal affinities of rodentia studied by sequence analysis of eye lens protein. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 211–226

    Google Scholar 

  35. Karita A, Blanchard J, Fortner JG (1975) Hamster to rat cardiac xenografts: a useful model for transplantation studies. J Surg Res 19: 99–102

    Google Scholar 

  36. Knechtle SJ, Haperin EC, Bollinger ER (1987) Xenograft survival in two species combinations using total-lymphoid irradiation and cyclosporine. Transplantation 43: 173–177

    Google Scholar 

  37. Lavocat R (1962) Etudes systématiques sur la dentition des Muridés. Mammalia 21: 107–127

    Google Scholar 

  38. Lavocat R (1969) La systématique des rongeurs hystricomorphes et la dérive des continents. C R Acad Sci Paris 269: 1496–1497

    Google Scholar 

  39. Lavocat R (1973) Les rongeurs du Miocène du Kenya. Mem et Travaux de l'Institut de Montpellier de l'EPHE 1: 1–284

    Google Scholar 

  40. Lavocat R, Parent JP (1985) Phylogenetic analysis of middle ear features in fossil and living rodents. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 333–354

    Google Scholar 

  41. Lim SML, Li SQ, Wee A, Chong SM, Hu S, Rauff A, White D (1991) Both concordant and discordant heart xenografts are rejected by athymic (nude) rats with the same tempo as in T cell competent animals. Transplant Proc 23: 581–582

    Google Scholar 

  42. Luckett WP (1977) Ontogeny of amniote fetal membranes and their application to phylogeny. In: Hecht MK, Goody PC, Hecht BM (eds) Major patterns in vertebrate evolution. Plenum Press, New York, pp 439–516

    Google Scholar 

  43. Luckett WP (1985) Superordinal and intraordinal affinities of rodents: developmental evidence from the dentition and placentation. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 227–276

    Google Scholar 

  44. Luckett WP, Hartenberger JL (eds) (1985) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 1–721

    Google Scholar 

  45. Marchman W, Araneda D, De Masi R, Taylor D, Larkin E, Alqaisi M, Thomas F (1992) Prolongation of xenograft survival after combination therapy with 15 deoxyspergualin and total lymphoid irradiation in the hamster to rat cardiac xenograft model. Transplantation 53: 30–34

    Google Scholar 

  46. McKenna MC (1975) Toward a phylogenetic classification of the Mammalia. In: Luckett WP, Szalay FS (eds) Phylogeny of the primates. Plenum Press, New York, pp 21–46

    Google Scholar 

  47. Miller JFAP (1962) Rat skin grafts in mice. In: Wolsteholme GEW, Cameron MP (eds) Ciba Foundation symposium on transplantation, pp 384–388

  48. Miyagawa S, Horose H, Shirakura R, Naka Y, Nakata S, Kawashima Y, Seya T, Matsumoto M, Uenaka A, Kitamura H (1988) The mechanisms of discordant xenograft rejection. Transplantation 46: 825–830

    Google Scholar 

  49. Monden M, Valdivia LA, Gotoh M, Hasuike Y, Kubota N, Kanai T, Okamura J, Mori T (1987) Hamster to rat orthotopic liver transplantation. Transplantation 43: 745–750

    Google Scholar 

  50. Novacek JN (1992) Mammalian phylogeny: skaking the tree. Nature 356: 121–125

    Google Scholar 

  51. Parent JP (1980) Recherches sur l'oreille moyenne des rongeurs actuels et fossiles. Anatomie, valeur systématique. Thèse Etat, Université de Montpellier, pp 1–286

  52. Pruitt SK, Baldwin WM, Marsh HE, Lin SS, Yeh CG, Bollinger RR (1991) The effect of soluble complement receptor type 1 on hyperacute xenograft rejection. Transplantation 52: 868–873

    Google Scholar 

  53. Rosengard BR, Hall TS, Imagawa DK, Ueda K, Baumgartner WA, Borkon AM, Smith RRL, Hutchins GM (1985) Hyperacute rejection of cardiac xenografts: two new models showing differences in pathogenesis. Surg Forum 36: 361–362

    Google Scholar 

  54. Rosengard BR, Adachi H, Ueda K, Hall TS, Hutchins GM, Herskowitz A, Borkon AM, Baumgartner WA, Reitz BA (1986) Differences in the pathogenesis of first set allograft rejection and acute xenograft rejection as determined by sequential morphologic analysis. J Heart Transplant 5: 263–268

    Google Scholar 

  55. Rosengard BR, Hall TS, Hutchins GM, Baumgartner WA, Reitz BA (1986) Modification of the immune response to xenografts by donor and graft pretreatment. Transplant Proc 18: 449–451

    Google Scholar 

  56. Sakai K, Kountz SL (1976) Dissociation of humoral and cellular reactions of the rabbit, guinea pig and dog kidney xenografts in the rat. J Surg Res 21: 159–163

    Google Scholar 

  57. Sakakibara N, Click RE, Condie RM, Jamieson SW (1989) Rejection/acceptance of xenografts. Transplant Proc 21: 524–526

    Google Scholar 

  58. Sarich VM (1985) Rodent macromolecular systematics. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 423–452

    Google Scholar 

  59. Settaf A, Meriggi F, Stadt J van de, Gane P, Crougneau S, Reynes M, Rouger P, Houssin D (1987) Delayed rejection of liver xenografts compared to heart xenografts in rats. Transplant Proc 19: 1155–1157

    Google Scholar 

  60. Shoshani J, Goodman M, Czelusniak J, Braunitzer G (1985) A phylogeny of rodentia and other eutherian orders: parsimony analysis utilizing amino acid sequences of alpha and beta hemoglobin. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 191–210

    Google Scholar 

  61. Silberman H, Reckard CR, Klinman N, Barker CF (1972) Dependence of antilymphocyte serum effectiveness on the degree of donor recipient histocompatibility. Surg Forum 23: 303–306

    Google Scholar 

  62. Simpson GG (1945) The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85: 1–350

    Google Scholar 

  63. Stadt J van de, Vendeville B, Weill B, Crougneau S, Michel A, Filipponi F, Icard P, Renoux M, Louvel A, Houssin D (1988) Discordant heart xenografts in the rat: additional effect of plasma exchange and cyclosporine, cyclophosphamide or splenectomy in delaying hyperacute rejection. Transplantation 45: 514–518

    Google Scholar 

  64. Steinbrüchel DA, Madsen HH, Nielsen B, Kemp E, Larsen S, Koch C (1991) The effect of combined treatment with total lymphoid irradiation, cyclosporin A, and anti CD4 monoclonal antibodies in a hamster to rat heart transplantation model. Transplant Proc 23: 579–580

    Google Scholar 

  65. Sugimoto K, Shelby J, Corry RJ (1985) Effects of cyclosporine and blood transfusion on cardiac xenografts in combination of rat and mouse. Nippon Geka Gakkai Zasshi 86: 1444–1448

    Google Scholar 

  66. Szalay FS (1977) Phylogenetic relationships and a classification of the eutherian mammals. In: Hecht MK, Goody PC, Hecht BM (eds) Major patterns in vertebrate evolution. Plenum Press, New York, pp 315–374

    Google Scholar 

  67. Tavakoli R, Devaux JY, Nonnenmacher L, Louvel A, Weill B, Houssin D (1992) Discordant lung xenograft rejection in the rat. Transplantation 53: 235–237

    Google Scholar 

  68. Terasaki PI, Esail ML, Cannon JA, Longmire WP (1961) Destruction of lymphocytes in vitro by normal serum from common laboratory animals. J Immunol 87: 383–389

    Google Scholar 

  69. Termignon JL, Calmus Y, Chereau C, Kahan A, Houssin D, Weill B (1992) In vitro analysis of complement activation in xenogeneic hyperacute rejection. Transplant Proc 24: 443–444

    Google Scholar 

  70. Thomas FT, Marchman W, Carobbi A, Araneda D, Pryor W, Thomas J (1991) Immunobiology of the xenograft response: xenograft rejection in immunodeficient animals. Transplant Proc 23: 208–209

    Google Scholar 

  71. Valdivia LA, Monden M, Gotoh M, Hasuike Y, Kubota N, Ichikawa T, Okamura T, Mori T (1987) Prolonged survival of hamster to rat liver xenograft using splenectomy and ciclosporin administration. Transplantation 44: 759–763

    Google Scholar 

  72. Valdivia LA, Monden M, Gotoh M, Hasuike Y, Kubota N, Ichikawa T, Nakano Y, Okamura J, Mori T (1988) An important role for the spleen in rejection of hamster to rat xenografts. Transplant Proc 20: 329–331

    Google Scholar 

  73. Viegas-Péquinot E, Petit D, Benazzou T, Prod'homme M, Lombard M, Hoffschir F, Descailleaux J, Dutrillaux B (1986) Phylogénie chromosomique chez les sciuridae, gerbillidae, et muridae, et étude d'espèces appartenant à d'autres familles de rongeurs. Mammalia 50: 164–202

    Google Scholar 

  74. Weil R, Nozawa M, Weber C (1975) Cardiac heterotransplantation: morphological and immunohistological studies. Transplantation 19: 150–156

    Google Scholar 

  75. Wood AE (1958) Are there rodents suborders? Systematic Zoology 7: 169–173

    Google Scholar 

  76. Wood AE (1974) The evolution of the Old World and New World hystricomorphs. Symposia Zool Soc London 34: 21–60

    Google Scholar 

  77. Wood AE (1985) The relationships, origin and dispersal of the hystricognathous rodents. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 475–513

    Google Scholar 

  78. Woods CA, Hermanson JW (1985) Myology of hystricognath rodents: an analysis of form, function and phylogeny. In: Luckett WP, Hartenberger JL (eds) Evolutionary relationships among rodents. A multidisciplinary analysis. Plenum Press, New York, pp 515–548

    Google Scholar 

  79. Wyss AR, Novacek MJ, McKenna MC (1987) Amino acid sequence versus morphological data and the interordinal relationships of mammals. Mol Biol Evol 4: 99–116

    Google Scholar 

  80. Yamaguchi Y, Halperin EC, Mori K, Misumi M, Katsumori T, Takata N, Goto M, Makino Y, Kituchi N, Takahashi K, Bollinger RR (1991) Macrophage migration into hepatic xenografts in the hamster-to-rat combination. Transplant Proc 23: 220–221

    Google Scholar 

  81. Zhang J, Munda R, Glas-Greenwald P, Weiss MA, Pollak VE, Alexander JW (1983) Prolongation of survival of a heart xenograft by defibrination with ancrody. Transplantation 35: 620–624

    Google Scholar 

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  1. Didier Houssin

    Present address: Clinique Chirurgicale, Hôpital Cochin, 27, rue du Faubourg Saint-Jacques, F-75679, Paris Cedex 14, France

Authors and Affiliations

  1. Laboratoire de Paléontologie analytique et Géologie sédimentaire, URA CNRS 157, Université de Bourgogne, Dijon, France

    Jean Chaline

  2. Laboratoire de Préhistoire et Paléoécologie du Quaternaire de l'EPHE, Université de Bourgogne, Dijon, France

    Jean Chaline

  3. Laboratoire de Recherche Chirurgicale, UER Cochin Port-Royal, Paris, France

    Jorge Cardoso & Didier Houssin

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Chaline, J., Cardoso, J. & Houssin, D. Organ xenografting between rodents: an evolutionary perspective. Transplant Int 7, 216–222 (1994). https://doi.org/10.1007/BF00327090

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