Spallanzani's mouse: A model of restoration and regeneration

Current Topics in Microbiology and Immunology

Volumn 280, Issue , 2003, Pages 165-189

  Heber Katz, E ^a   Leferovich, J M ^a   Bedelbaeva, K ^a   Gourevitch, D ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; ENZYME INHIBITOR; GELATINASE A; GELATINASE B; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ANGIOGENESIS; BASEMENT MEMBRANE; BLASTEMA; EAR INJURY; ECHOCARDIOGRAPHY; EXTRACELLULAR MATRIX; GENE LOCUS; GENETIC ANALYSIS; HEALING; HEART RIGHT VENTRICLE; MACROPHAGE; MAMMAL; MODEL; MOUSE; MOUSE STRAIN; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT; REGENERATION; REVIEW; SCAR; SCAR FORMATION; SPALLANZANI MOUSE; TISSUE REGENERATION;

ANIMALS; BASEMENT MEMBRANE; EAR; EXTRACELLULAR MATRIX; HEART; MICE; MICE, INBRED MRL LPR; MODELS, ANIMAL; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; QUANTITATIVE TRAIT LOCI; REGENERATION; STEM CELLS; WOUND HEALING;

AMPHIBIA; MAMMALIA;

EID: 0141705550     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: None     Document Type: Review

References (107)

1. Anversa P, Nadal-Ginard B (2002) Myocyte renewal and ventricular remodelling. Nature 415:240-243
2. Anversa P, Nadal-Ginard B. (2002a) Cardiac chimerism: methods matter. Circulation. 106:129-31
3. Adachi M, Watanabe-Fukunaga R, Nagata S. (1993) Aberrant transcription caused by the insertion of an endogenous retrovirus in an apoptosis gene. Proc. Natl. Acad. Sci. USA 90:1756-1760
4. Battegay EJ. (1995). Angiogenesis: mechanistic insights, neovascular diseases, and therapeutic prospects. J Mol Med. 73:333-46
5. Bauer SR, Ruiz-Hidalgo MJ, Rudikoff EK, Goldstein J, Laborda J. (1998) Modulated expression of the epidermal growth factor-like homeotic protein dlk influences stromal-cell-pre-B-cell interactions, stromal cell adipogenesis, and pre-B-cell interleukin-7 requirements. Mol Cell Biol 1998; 18:5247-55
6. Beltrami, A.P., Urbanek, K., Kajstura, J., Yan, S-M., Finato, N., Bussani, R., Nadal-Ginard, B., Silvestri, F., Leri, A, Beltrami, C.A., and Anversa, P. (2001) Evidence that human cardiac myocytes divide after myocardial infarction. New Engl J. Med. 344:1750-1757
7. Blankenhorn, E.P., Troutman, S., Desquennes-Clark, L., Zhang, X-M., and Heber-Katz, E. (2003) Sexually dimorphic genes regulate healing and regeneration in the MRL/MpJ mouse. Mammalian Genome. 14:250-260
8. Borgens, R.B. (1982) Mice regrow the tips of the foretoes. Science 217:747-50
9. Borisov, A.B. (1998) Cellular mechanisms of myocardial regeneration in Cellular and Molecular Basis of Regeneration from Invertebrates to Humans. eds. Ferretti, P and Geraudie, J. (John Wiley and Sons Ltd., Chichester,). pp.335-354
10. Borisov, A. (1999) Regeneration of skeletal and cardiac muscle in mammals: do non-primate models resemble human pathology? Wound Rep. Regen. 7:26-35
11. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636 40
12. Brockes J.P. (1997) Amphibian limb regeneration: rebuilding a complex structure. Science 276:81-87
13. Brockes JP, Kumar A. (2002) Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat Rev Mol Cell Biol. 3:566-74
14. Cadinouche MZ, Liversage RA, Muller W, Tsilfidis C.(1999) Molecular cloning of the Notophthalmus viridescens radical fringe cDNA and characterization of its expression during forelimb development and adult forelimb regeneration. Dev Dyn. 214:259-68
15. Carbone, A, Minieri, M, Sampaolesi, M, Fiaccavento, R., De Feo, A., Cesaroni, P, Peruzzi, G., Di Nardo, P. (1995). Hamster Cardiomyocytes: a model of myocardial regeneration? Annals of the New York Academy of Sciences. 752:75-71
16. Chernoff EAG, O'Hara CM, Bauerle B, Bowling M. (2000) Matrix metalloproteinase production in regenerating axolotl spinal cord. Wound Repair Regen 8:282-291
17. Chernoff E, Sato K, Corn A, Karcavich R. (2002) Spinal cord regeneration: intrinsic properties and emerging mechanisms. Semin Cell Dev Biol. 13:361
18. Christensen RN, Weinstein M, Tassava RA. (2002) Expression of fibroblast growth factors 4, 8, and 10 in limbs, flanks, and blastemas of Ambystoma. Dev Dyn. 223:193-203
19. Clark, L., Clark, R., and Heber-Katz, E. (1998) A new model for mammalian wound repair and regeneration. Clin. Immun. Immunopath. 88:35-45
20. Clark, R.A.F. (1996) Wound repair: overview and general consideration. In: The Molecular and Cellular Biology of Wound Repair. (R.Clark, ed.). Plenum Press, NY. pp.3-35
21. Cohen, P.L. and Eisenberg, R.A. (1991). Lpr and gld; Single Gene models of Systemic Autoimmunity and Lymphoproliferartive disease. Annu. Rev. Immunol. 9, 243-69
22. Condic ML, Lemons ML (2002) Extracellular matrix in spinal cord regeneration: getting beyond attraction and inhibition. Neuroreport 13:A37-48
23. Condorelli G, Borello U, De Angelis L, Latronico M, Sirabella D, Coletta M, Galli R, Balconi G, Follenzi A, Frati G, Cusella De Angelis MG, Gioglio L, Amuchastegui S, Adorini L, Naldini L, Vescovi A, Dejana E, Cossu G (2001) Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: implications for myocardium regeneration. Proc Natl Acad Sci U S A 98:10733-8
24. Davies SJ, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822
25. Dickie MM. Keeping Records, p25. In Biology of the Laboratory Mouse. Green EL (ed), Dover Publications. New York, 1975
26. Dinsmore, CE. (ed) (1991) A History of Regeneration Research: Milestones in the Evolution of a Science. Cambridge University Press. New York
27. Dixon, IMC, Haisong, J, Reid, NL, Scammell-La Fleur, T, Werner, JP, and Jasmin, G. (1997) Cardiac collagen remodeling in the cardiomyopathic syrian hamster and the effect of losartan. J. Mol Cell Cardiol. 29:1837-1850
28. Douglas BS (1972) Conservative management of guillotine amputations of the fingers of children. Austral Paediatr J 8:86-90
29. Dresden MH, Gross J. (1970) The collagenolytic enzyme of the regenerating limb of the Newt Triturus viridescens. Dev Biol. 22:129-37
30. Echeverri K, Clarke JDW, and Tanaka E. (2001) In vivo Imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. Developmental Biology 236:151-164
31. Folkman, J. and Klagsbrun, M. (1987) Angiogenic factors. Science 235, 442-447
32. Garces C, Ruiz-Hidalgo MJ, Bonvini E, Goldstein J, Laborda J. (1999) Adipocyte differentiation is modulated by secreted delta-like (dlk) variants and requires the expression of membrane-associated dlk. Differentiation 64:103-14
33. Gardiner, D.M. and Bryant, S.V. (1996) Molecular mechanisms in the control of limb regeneration: the role of homeobox genes. Int. J. Dev. Biol. 40:797-805
34. Globus M, Vethamany-Globus S, Lee YCI. (1980) Effect of apical epidermal cap on mitotic cycle and cartilage differentiation in regeneration blastemata in the newt. Notophthalmus viridescens. Develop Biol 75:358-372
35. Gourevitch, D, Clark, L, Chen P, Seitz A, Samulewicz S, and E. Heber-Katz. (2003) Matrix Metalloproteinase Activity Correlates with Blastema Formation in the Regenerating MRL Mouse Ear Hole Model. Dev Dyn. 226:377-287
36. Grillo HC, Lapiere CM, Dresden MH, Gross J. (1968) Collagenolytic activity in regenerating forelimbs of the adult newt. Dev Biol 17:571-583
37. Gross, J. (1996) Getting to mammalian wound repair and amphibian limb regeneration: a mechanistic link in the early events. Wound Repair Reg. 4:190-202
38. Grounds MD, White JD, Rosenthal N, Bogoyevitch MA (2002) The role of stem cells in skeletal and cardiac muscle repair. J Histochem Cytochem. 50:589-610
39. Goss, R.J. (1970) Problems of antlerogenesis. Clin. Orthopaedics 69:227-238
40. Goss, R.J. and Grimes, L.N. (1975) Epidermal downgrowths in regenerating rabbit ear holes. J. Morphol. 146:533-542
41. Gourevich, D, Clark, L, Chen P, Seitz A, Samulewicz S, and E. Heber-Katz. (2003) Matrix Metalloproteinase Activity Correlates with Blastema Formation in the Regenerating MRL Ear Hole Model. Developmental Dynamics. 226:377-387
42. Heymans S, Luttun A, Nuyens D, Theilmeier G, Creemers E, Moons L, Dyspersin GD, Cleutjens JP, Shipley M, Angellilo A, Levi M, Nube O, Baker A, Keshet E, Lupu F, Herbert JM, Smits JF, Shapiro SD, Baes M, Borgers M, Collen D, Daemen MJ, Carmeliet P. (1999) Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure. Nature Medicine 5:1135-1142
43. Heber-Katz, E. (1999) The regenerating mouse ear. Sem. Cell Dev. Biol. 10:415-420
44. Heber-Katz, E., Chen, P., Clark, L., Zhang, X-M., Troutman, S., and Blankenhorn, EP. (2002) Novel genetic loci associated with wound healing and regeneration that distinguish MRL and M. m. castaneus mice. Submitted
45. Illingworth CM (1974) Trapped fingers and amputated finger tips in children. J Pediatr Surg 9:853-58
46. Isner, JM. (2002) Myocardial gene therapy. Nature 415:234-239
47. Jackson KA, Majika SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell M (2001) Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Inv 107:1395-1402
48. Kalkman EA, Bilgin YM, van Haren P, van Suylen RJ, Saxena PR, Schoemaker RG. (1996) Determinants of coronary reserve in rats subjected to coronary artery ligation or aortic banding. Cardiovasc.Res. 32, 1088-1095
49. Kaneko Y, Hirota K, Matsumoto G, Hanyu Y. (2001) Expression pattern of a newt Notch homologue in regenerating newt retina. Brain Res Dev Brain Res. 128:53-62
50. Kench, J.A., Russell, D.M., Fadok, V.A., Young, S.K., Worthen, G.S., Jones-Carsen, J., Henson, J.E., Henson, P.M., and Nemazee, D. (1999) Aberrant wound healing and TGF-beta production in the autoimmune-prone MRL/+ mouse. Clin. Immunol. 92:300-310
51. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. (2001) Neovascularization of ischemic myocardium by human bone marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling, and improves cardiac function. Nature Medicine 7:430-436
52. Laflamme MA, Myerson D, Saffitz JE, Murry CE. (2002) Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 90:634-40
53. Lee, JK, Zaidi, SHE, Liu, P., Dawood, F, Cheah, AYL, Wen, W-H, Saiki, Y., and Rabinovitch, M. (1998) A serine esterase inhibitor reduces inflammation and fibrosis and preserves cardiac function after experimentally-induced murine myocarditis. Nature Medicine 4:1383-1391
54. Leferovich, J., Bedelbaeva, K., Samulewicz, S, Xhang, X-M, Zwas, DR, Lankford, EB, and Heber-Katz, E. (2001) Heart regeneration in adult MRL mice. Proc. Natl. Acad. Sci. USA, 98:9830-9835
55. Li, X., Gu, W., Masinde, G., Hamilton-Ulland, M., Xu, S., Mohan, S., and Baylink, D.J. (2001) Genetic control of the rate of wound healing in mice. Heredity. 86:668-674
56. Li, YY, Feng, YQ, Kadokami, T, McTiernan, CF, Draviam, R, Watkins, SC, and Feldman AM. (2000) Mycardial extracellular matrix remodeling in transgenic mice overexpressing tumor necrosis factor alpha can be modulated by anti-tumor necrosis factor alpha therapy. PNAS 97:12746-12751
57. Lo D, Allen F, Brockes JP. (1993) Reversal of muscle differentiation during urodele limb regeneration. PNAS 90:7230-7234
58. Mauro, A. 1961. Satellite cell of skeletal muscle fibres. J Biophys Biochem Cytol 9:493 498
59. Masinde, G.L., Li, X., Gu, W., Davidson, H., Mohan, S., and Baylink, D.J. (2001) Identification of wound healing/regeneration quantitative trait loci (QTL) at multiple time points that explain seventy percent of variance in (MRL/MpJ and SJL/J) mice F2 population. Genome Res. 11:2027-2033
60. McBrearty, B.A., Desquenne-Clark, L., Zhang, X-M., Blankenhorn, E.P., and Heber-Katz, E. (1998) Genetic analysis of a mammalian wound healing trait. Proc. Natl. Acad. Sci. USA, 95:11792-11797
61. Miyazaki, K, Uchiyawa K, Imokawa Y, Yoshizato K. (1996) Cloning and characterization of cDNAs for matrix metalloproteinases of regenerating newt limbs. Proc Natl Acad Sci USA 93:6819-6824
62. Morris RJ, and Potten CS. (1994) Slowly cycling label-retaining epidermal cells behave like clonogenic stem cells in vitro Cell Prolif. 27:279-289
63. Moss and Leblond (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec. 170:421-35
64. Murphy, E.D. and Roths, J.B. (1979) Autoimmunity and lymphoproliferation: Induction by mutant gene lpr and acceleration by a male-associated factor in strain BXSB. in Genetic Control of Autoimmune Disease. (eds. Rose, N.R., Bigazzi, P.E., and Warner, N.L.) 207-220 (Elsevier, New York)
65. Nadal-Ginard,B. (1978) Comittment, fusion, and biochemical differentiation of a myogenic cell line in the absence of DNA synthesis. Cell. 15:855-864
66. Nelissen-Vrancken HJ, Debets JJ, Snoeckx LH, Daemen MJ, Smits JF. (1996) Time-related normalization of maximal coronary flow in isolated perfused hearts of rats with myocardial infarction. Circulation. 1996 93:349-55
67. Neufield DA (1989) Epidermis, basement membrane, and connective-tissue healing after amputation of mouse digits: implications for mammalian appendage regeneration. Anat Rec 223:425-32
68. Newmark PA, Sanchez Alvarado A. (2002) Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genet. 3:210-9
69. Oberpriller, JO, Ferrans, VJ, McDonnell, TJ, and Oberpriller, JC. (1985) Activation of DNA synthesis and mitotic events in atrial myocytes following atrial and ventricular injury. in Pathobiology of Cardiovascular Injury. Ed.Stone and Weglicki, (Martinus Nijhoff Publishing, Boston) pp. 410-421
70. Odelberg SJ, Kollhoff A, and Keating MT. (2000) Dedifferentiation of Mammalian Myotubes Induced by msxl. Cell 103:1099-1109
71. Orlic, D, et al. (2001a) Bone marrow cells regenerate infarcted myocardium. nature. 410:701-5
72. Orlic D et al. (2001b) Mobilized bone marrow cells repair the infarcted heart, improving function and survival. PNAS. 98:10344-10349
73. Polezhaev, L.V. (1972) Loss and Restoration of Regenerative Capacity in Tissues and Organs of Animals ed. Polezhaev LV (Harvard University Press, Cambridge). pp. 153-199
74. Popova, NV, Tryson K, Wu K, and Morris RJ. (2002) Evidence that keratinocyte colony number is genetically controlled. Exp Dermatol. 11:503-508
75. Popova NV, Teti KA, Wu KQ, Morris RJ. Identification of two keratinocyte stem cell regulatory loci implicated in skin carcinogenesis. Carcinogenesis (2003) 24(3):417-25
76. Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kajstura J, Leri A, Anversa P. (2002) Chimerism of the transplanted heart. N Engl J Med. 346:5-15
77. Quinones JL, Rosa R, Ruiz DL, Garcia-Arraras JE. (2002) Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol. 250:181-97
78. Reginelli AD, Wang YQ, Sassoon D, Muneoka K.1995. Digit tip regeneration correlates with regions of Msx1 (Hox 7) expression in fetal and newborn mice regrowth. Development 121:1065-76
79. Repesh LA, Oberpriller JC. (1980) Ultrastructural studies on migrating epidermal cells during the wound healing stage of regeneration in the adult newt, Notophthalmus viridescens. Am J Anat. 159:187-208
80. Rumyantev, PP. (1973) Post-injury DNA synthesis, mitosis, and ultrastructural reorganization of adult frog cardiac myocytes. Z. Zellforsch. 139:431-450
81. Samulewicz, SJ, Clark, L, Seitz, A., and E. Heber-Katz. (2002) Expression of Pref-1, A Delta-Like Protein, in Healing Mouse Ears. Wound Repair and Regeneration, 10:215-221
82. Sasayama, S. and Fujita, M. (1992) Recent insights into coronary collateral circulation. Circulation, 85:1197-1204
83. Sawada T, Oofusa K, Yoshizato K. (1999) Characterization of a collagenolytic enzyme released from wounded planarians dugesia japonica. Wound Rep Regen 7:458-466
84. Scheuer J, Buttrick P. (1987) The cardiac hypertrophic responses to pathologic and physiologic loads. Circulation. 75:163-8
85. Seitz, A., Aglow, E., and Heber-Katz, E. (2002) Recovery from spinal cord injury: A new transection model in the C57B1/6 mouse. J. Neuroscience Research. 67:337-345
86. Seitz, A, Kragol, M, Aglow, E, Showe, L. and E, Heber-Katz. (2003) Apo-E expression after spinal cord injury in the mouse. J. Neuroscience Research. 71:417-426
87. Smas CM, Sul HS. (1993) Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell 73:725-34
88. Stichel CC, Niermann H, D'Urso D, Lausberg F, Hermanns S, Muller HW (1999) Basal membrane-depleted scar in lesioned CNS: characteristics and relationships with regenerating axons. Neurosci 93:321-33
89. Song, W., Jackson, K., and McGuire, P.G. (2000) Degradation of Type IV Collagen by Matrix Metalloproteinases is an important step in the epithelial-mesenchymal transformation of the endocardial cushions. Develop Biol. 227:606-617
90. Stocum, D.L. (1984) The urodele limb regeneration blastema. Determination and organization of the morphogenetic field. Differentiation 27:13-28
91. Stocum, D.L. (1996) Tissue restoration: approaches and prospects. Wound Repair Reg. 4:3-15
92. Stocum DL and Crawford, K (1987) Use of retinoids to analyze the cellular basis of positional memory in regenerating amphibian limbs. Biochem Cell Biol. 65:750-61
93. Stocum DL and Dearlove GE. (1972) Epidermal-mesodermal interaction during morphogenesis of the limb regeneration blastema in larval salamanders. J. Exp. Zool. 181:49-62
94. Sun, Y, and Weber, KT. (2000) Infarct scar: a dynamic tissue. Cardiovacular Research. 46:250-6
95. Tabin, C.J. (1991) Retinoids, homeoboxes, and growth factors: towards molecular models for limb development. Cell 66:199-217
96. Taylor, D.A., Atkins, B.Z., Hungspreugs, P., Jones, T.R., Reedy, M.C., Hutcheson, K. A., Glower, D.D. and Kraus, W.E. (1998) Regenerating functional myocardium: improved performance after skeletal myoblast transplantation. Nature Medicine, 4:929-933
97. Taylor DA, Hruban R, Rodriguez ER, Goldschmidt-Clermont PJ (2002) Cardiac chimerism as a mechanism for self-repair: does it happen and if so to what degree? Circulation. 106:2-4
98. Technau U, Cramer von Laue C, Rentzsch F, Luft S, Hobmayer B, Bode HR, Holstein TW (2000) Parameters of self-organization in Hydra aggregates. Proc Natl Acad Sci 97:12127-31
99. Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, Meyer EM, Morel L, Petersen BE, Scott EW (2002) Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416:542-5
100. Theofilopoulos, A.N. Immunologic genes in mouse lupus models (1993) in: The Molecular Pathology of Autoimmune Diseases. (eds. Bona, C., Siminovitch, K.A., Zanetti, M. and Theofilopoulos, A.N.) 281-316 (Harwood Academic Publishers, Langhorne)
101. Toma, C, Pittenger, MF, Cahill KS, Byrne BJ, Kessler P (2002) Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 105:93-98
102. Vracko, R. and Thorning, D (1985) Freeze-thaw injury of rat heart across an intact diaphragm: a new model for the study of the response of myocardium to injury. Cardiovasc Res., 19:76-84
103. Watanabe-Fukunaga, R., Brannan, C., Copeland, N.G., Jenkins, N.A., and Nagata, S (1992) Lymphoproliferation disorder in mice is explained by defects in Fas antigen that mediates apoptosis. Nature 356:314-316
104. Watson ML, Rao JK, Gilkeson GS, Ruiz P, Eicher EM, Pisetsky DS, Matsuzawa A, Rochelle JM, Seldin MF (1992) Genetic analysis of MRL-lpr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease modifying loci. J. Exp. Med. 176, 1645-1656
105. Warejcka DJ, Harvey R, Taylor BJ, Young HE, Lucas PA (1996) A population of cells isolated from rat heart capable of differentiating into several mesodermal phenotypes. J Surg Res 62:233-242
106. Yang EV, Bryant SV (1994) Developmental regulation of a matrix metalloproteinase during regeneration of axolotl appendages. Dev Biol 166:696-703
107. Zammit PS, Heslop L, Hudon V, Rosenblatt JD, Tajbakhsh S, Buckingham ME, Beauchamp JR, Partridge TA (2002) Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibers. Exp Cell Res 281:39-49