Molecular insight into the association between cartilage regeneration and ear wound healing in genetic mouse models: Targeting new genes in regeneration

G3: Genes, Genomes, Genetics

Volumn 3, Issue 11, 2013, Pages 1881-1891

  Rai, Muhammad Farooq ^a   Schmidt, Eric J ^a   McAlinden, Audrey ^a   Cheverud, James M ^a   Sandell, Linda J ^a  

^a BARNES JEWISH HOSPITAL   (United States)

Author keywords

Articular cartilage; Assay; Inbred lines; Osteoarthritis; Quantigene Plex; Recombinant; Regeneration; Tissue

Indexed keywords

AXIN; AXIN2 PROTEIN; CYCLINE; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; WNT16 PROTEIN; XRCC2 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BIOINFORMATICS; CONTROLLED STUDY; DNA REPAIR; GENE; GENE EXPRESSION; GENE MAPPING; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HERITABILITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PHENOTYPE; RECOMBINANT INBRED STRAIN; SEQUENCE ANALYSIS; TISSUE REGENERATION; TISSUE SECTION; WNT SIGNALING PATHWAY; WOUND HEALING;

ARTICULAR CARTILAGE; OSTEOARTHRITIS; QUANTIGENE PLEX ASSAY; RECOMBINANT INBRED LINES; TISSUE REGENERATION;

ANIMALS; AXIN PROTEIN; CARTILAGE; COMPUTATIONAL BIOLOGY; DNA REPAIR; DNA-BINDING PROTEINS; EAR; MICE; MICRORNAS; MODELS, GENETIC; OSTEOARTHRITIS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROLIFERATING CELL NUCLEAR ANTIGEN; REGENERATION; TRANSCRIPTOME; WNT PROTEINS; WOUND HEALING;

EID: 84889077390     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.007302     Document Type: Article

References (70)

1. Adzhubei, I., D. M. Jordan, and S. R. Sunyaev, 2013 Predicting functional effect of human missense mutations using PolyPhen-2. Curr. Protoc. Hum. Genet. Chapter 7: Unit7.20
2. Adzhubei, I. A., S. Schmidt, L. Peshkin, V. E. Ramensky, A. Gerasimova et al., 2010 A method and server for predicting damaging missense mutations. Nat. Methods 7: 248-249
3. Baron, R., and G. Rawadi, 2007 Targeting the Wnt/beta-catenin pathway to regulate bone formation in the adult skeleton. Endocrinology 148: 2635-2643
4. Bedelbaeva, K., A. Snyder, D. Gourevitch, L. Clark, X. M. Zhang et al., 2010 Lack of p21 expression links cell cycle control and appendage regeneration in mice. Proc. Natl. Acad. Sci. USA 107: 5845-5850
5. Bely, A. E., 2010 Evolutionary loss of animal regeneration: pattern and process. Integr. Comp. Biol. 50: 515-527
6. Blankenhorn, E. P., G. Bryan, A. V. Kossenkov, L. D. Clark, X. M. Zhang et al., 2009 Genetic loci that regulate healing and regeneration in LG/J and SM/J mice. Mamm. Genome 20: 720-733
7. Bresters, D., M. E. Schipper, H. W. Reesink, B. D. Boeser-Nunnink, and H. T. Cuypers, 1994 The duration of fixation influences the yield of HCV cDNA-PCR products from formalin-fixed, paraffin-embedded liver tissue. J. Virol. Methods 48: 267-272
8. Carames, B., A. Hasegawa, N. Taniguchi, S. Miyaki, F. J. Blanco et al., 2012 Autophagy activation by rapamycin reduces severity of experimental osteoarthritis. Ann. Rheum. Dis. 71: 575-581
9. Carames, B., N. Taniguchi, S. Otsuki, F. J. Blanco, andM. Lotz, 2010 Autophagy is a protective mechanism in normal cartilage, and its aging-related loss is linked with cell death and osteoarthritis. Arthritis Rheum. 62: 791-801
10. Carlson, B. M., 2005 Some principles of regeneration in mammalian systems. Anat. Rec. B New Anat. 287: 4-13
11. Chan, E. Y., S. Kir, and S. A. Tooze, 2007 siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J. Biol. Chem. 282: 25464-25474
12. Choi, J., M. Jo, E. Lee, Y. K. Oh, and D. Choi, 2012 The role of autophagy in human endometrium. Biol. Reprod. 86: 70
13. Chun, S., and J. C. Fay, 2009 Identification of deleterious mutations within three human genomes. Genome Res. 19: 1553-1561
14. Clark, L. D., R. K. Clark, and E. Heber-Katz, 1998 A new murine model for mammalian wound repair and regeneration. Clin. Immunol. Immunopathol. 88: 35-45
15. Colwell, A. S., T. M. Krummel, W. Kong, M. T. Longaker, and H. P. Lorenz, 2006 Skin wounds in the MRL/MPJ mouse heal with scar. Wound Repair Regen. 14: 81-90
16. Colwell, A. S., M. T. Longaker, and H. P. Lorenz, 2005 Mammalian fetal organ regeneration. Adv. Biochem. Eng. Biotechnol. 93: 83-100
17. Cuervo, R., R. Hernandez-Martinez, J. Chimal-Monroy, H. Merchant-Larios, and L. Covarrubias, 2012 Full regeneration of the tribasal Polypterus fin. Proc. Natl. Acad. Sci. USA 109: 3838-3843
18. Dao, D. Y., X. Yang, L. M. Flick, D. Chen, M. J. Hilton et al., 2010 Axin2 regulates chondrocyte maturation and axial skeletal development. J. Orthop. Res. 28: 89-95
19. de Hooge, A. S., F. A. van De Loo, O. J. Arntz, and W. B. van Den Berg, 2000 Involvement of IL-6, apart from its role in immunity, in mediating a chronic response during experimental arthritis. Am. J. Pathol. 157: 2081-2091
20. Dell'accio, F., C. De Bari, N. M. Eltawil, P. Vanhummelen, and C. Pitzalis, 2008 Identification of the molecular response of articular cartilage to injury, by microarray screening: Wnt-16 expression and signaling after injury and in osteoarthritis. Arthritis Rheum. 58: 1410-1421
21. Falconer, D. S., and T. F. C. Mackay, 1996 Introduction to Quantitative Genetics, Ed. 4. Longmans Green, Harlow, Essex, UK
22. Fini, M. E., 1999 Keratocyte and fibroblast phenotypes in the repairing cornea. Prog. Retin. Eye Res. 18: 529-551
23. Finke, J., R. Fritzen, P. Ternes, W. Lange, and G. Dolken, 1993 An improved strategy and a useful housekeeping gene for RNA analysis from formalin-fixed, paraffin-embedded tissues by PCR. Biotechniques 14: 448-453
24. Fitzgerald, J., C. Rich, D. Burkhardt, J. Allen, A. S.Herzka et al., 2008 Evidence for articular cartilage regeneration in MRL/MpJ mice. Osteoarthritis Cartilage 16: 1319-1326
25. Gierer, A., S. Berking, H. Bode, C. N. David, K. Flick et al., 1972 Regeneration of hydra from reaggregated cells. Nat. New Biol. 239: 98-101
26. Gurtner, G. C., S. Werner, Y. Barrandon, and M. T. Longaker, 2008 Wound repair and regeneration. Nature 453: 314-321
27. Harty, M., A. W. Neff, M. W. King, and A. L. Mescher, 2003 Regeneration or scarring: an immunologic perspective. Dev. Dyn. 226: 268-279
28. Hashimoto, S., M. F. Rai, K. L. Janiszak, J. M. Cheverud, and L. J. Sandell, 2012 Cartilage and bone changes during development of post-traumatic osteoarthritis in selected LGXSM recombinant inbred mice. Osteoarthritis Cartilage 20: 562-571
29. Heber-Katz, E., 1999 The regenerating mouse ear. Semin. Cell Dev. Biol. 10: 415-419
30. Heydemann, A., K. A. Swaggart, G. H. Kim, J. Holley-Cuthrell, M. Hadhazy et al., 2012 The superhealing MRL background improves muscular dystrophy. Skelet Muscle 2: 26
31. Hrbek, T., R. A. de Brito, B. Wang, L. S. Pletscher, and J. M. Cheverud, 2006 Genetic characterization of a new set of recombinant inbred lines (LGXSM) formed from the inter-cross of SM/J and LG/J inbred mouse strains. Mamm. Genome 17: 417-429
32. Kench, J. A., D. M. Russell, V. A. Fadok, S. K. Young, G. S. Worthen et al., 1999 Aberrant wound healing and TGF-beta production in the autoimmune-prone MRL/+ mouse. Clin. Immunol. 92: 300-310
33. Kierdorf, U., and H. Kierdorf, 2011 Deer antlers-a model of mammalian appendage regeneration: an extensive review. Gerontology 57: 53-65
34. Kim, J., M. Xu, R. Xo, A. Mates, G. L. Wilson et al., 2010 Mitochondrial DNA damage is involved in apoptosis caused by pro-inflammatory cytokines in human OA chondrocytes. Osteoarthritis Cartilage 18: 424-432
35. Knudsen, B. S., A. N. Allen, D. F. McLerran, R. L. Vessella, J. Karademos et al., 2008 Evaluation of the branched-chain DNA assay for measurement of RNA in formalin-fixed tissues. J. Mol. Diagn. 10: 169-176
36. Kumar, P., S. Henikoff, and P. C. Ng, 2009 Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4: 1073-1081
37. Kundu, M., T. Lindsten, C. Y. Yang, J. Wu, F. Zhao et al., 2008 Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood 112: 1493-1502
38. Li, X., W. Gu, G. Masinde, M. Hamilton-Ulland, S. Xu et al., 2001 Genetic control of the rate of wound healing in mice. Heredity (Edinb) 86: 668- 674
39. Loeser, R. F., A. L. Olex, M. A. McNulty, C. S. Carlson, M. F. Callahan et al., 2012 Microarray analysis reveals age-related differences in gene expression during the development of osteoarthritis in mice. Arthritis Rheum. 64: 705-717
40. Logan, C. Y., and R. Nusse, 2004 The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20: 781-810
41. Macabeo-Ong, M., D. G. Ginzinger, N. Dekker, A. McMillan, J. A. Regezi et al., 2002 Effect of duration of fixation on quantitative reverse transcription polymerase chain reaction analyses. Mod. Pathol. 15: 979-987
42. Masinde, G. L., R. Li, B. Nguyen, H. Yu, A. K. Srivastava et al., 2006 New quantitative trait loci that regulate wound healing in an intercross progeny from DBA/1J and 129 x 1/SvJ inbred strains of mice. Funct. Integr. Genomics 6: 157-163
43. Masuda, N., T. Ohnishi, S. Kawamoto, M. Monden, and K. Okubo, 1999 Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples. Nucleic Acids Res. 27: 4436-4443
44. Matullo, G., S. Guarrera, C. Sacerdote, S. Polidoro, L. Davico et al., 2005 Polymorphisms/haplotypes in DNA repair genes and smoking: a bladder cancer case-control study. Cancer Epidemiol. Biomarkers Prev. 14: 2569-2578
45. McBrearty, B. A., L. D. Clark, X. M. Zhang, E. P. Blankenhorn, and E. Heber-Katz, 1998 Genetic analysis of a mammalian wound-healing trait. Proc. Natl. Acad. Sci. USA 95: 11792-11797
46. Metcalfe, A. D.,H.Willis, A. Beare, andM.W. Ferguson, 2006 Characterizing regeneration in the vertebrate ear. J. Anat. 209: 439-446
47. Moreno, V., F. Gemignani, S. Landi, L. Gioia-Patricola, A. Chabrier et al., 2006 Polymorphisms in genes of nucleotide and base excision repair: risk and prognosis of colorectal cancer. Clin. Cancer Res. 12: 2101-2108
48. Murphy, E. D., and J. B. Roths, 1979 Autoimmunity and lymphoproliferation: Induction by mutant gene lpr and acceleration by a male-associated factor in strain BXSB, pp. 207-220 in Genetic Control of Autoimmune Disease, edited by N. R. Rose, P. E. Bigazzi, and N. L. Warner. Elsevier, New York
49. Natsuka, S., S. Akira, Y. Nishio, S. Hashimoto, T. Sugita et al., 1992 Macrophage differentiation-specific expression of NF-IL6, a transcription factor for interleukin-6. Blood 79: 460-466
50. Ohshima, S., Y. Saeki, T. Mima, M. Sasai, K. Nishioka et al., 1998 Interleukin 6 plays a key role in the development of antigen-induced arthritis. Proc. Natl. Acad. Sci. USA 95: 8222-8226
51. Okazaki, K., J. Li, H. Yu, N. Fukui, and L. J. Sandell, 2002 CCAAT/enhancerbinding proteins beta and delta mediate the repression of gene transcription of cartilage-derived retinoic acid-sensitive protein induced by interleukin-1 beta. J. Biol. Chem. 277: 31526-31533
52. Okazaki, K., H. Yu, S. R. Davies, T. Imamura, and L. J. Sandell, 2006 A promoter element of the CD-RAP gene is required for repression of gene expression in non-cartilage tissues in vitro and in vivo. J. Cell. Biochem. 97: 857-868
53. Park, Y. N., K. Abe, H. Li, T. Hsuih, S. N. Thung et al., 1996 Detection of hepatitis C virus RNA using ligation-dependent polymerase chain reaction in formalin-fixed, paraffin-embedded liver tissues. Am. J. Pathol. 149: 1485-1491
54. Rai, M. F., S. Hashimoto, E. E. Johnson, K. L. Janiszak, J. Fitzgerald et al., 2012 Heritability of articular cartilage regeneration and its association with ear wound healing in mice. Arthritis Rheum. 64: 2300-2310
55. Rai, M. F., D. Patra, L. J. Sandell, and R. H. Brophy, 2013 Transcriptome analysis of injured human meniscus reveals a distinct phenotype of meniscus degeneration with aging. Arthritis Rheum. 65: 2090-2101
56. Sanchez Alvarado, A., and P. A. Tsonis, 2006 Bridging the regeneration gap: genetic insights from diverse animal models. Nat. Rev. Genet. 7: 873- 884
57. Seifert, A. W., J. R. Monaghan, M. D. Smith, B. Pasch, A. C. Stier et al., 2012 The influence of fundamental traits on mechanisms controlling appendage regeneration. Biol. Rev. Camb. Philos. Soc. 87: 330-345
58. Stocum, D. L., 1984 The urodele limb regeneration blastema. Determination and organization of the morphogenetic field. Differentiation 27: 13- 28
59. Stoick-Cooper, C. L., G. Weidinger, K. J. Riehle, C. Hubbert, M. B. Major et al., 2007 Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134: 479-489
60. Tanaka, E. M., 2003 Regeneration: if they can do it, why can't we? Cell 113: 559-562
61. Tchetina, E. V., 2011 Developmental mechanisms in articular cartilage degradation in osteoarthritis. Arthritis (Egypt) 2011: 683970
62. ten Koppel, P. G., G. J. van Osch, C. D. Verwoerd, and H. L. Verwoerd-Verhoef, 2001 A new in vivo model for testing cartilage grafts and biomaterials: the 'rabbit pinna punch-hole' model. Biomaterials 22: 1407- 1414
63. Urdea, M. S., T. Horn, T. J. Fultz, M. Anderson, J. A. Running et al., 1991 Branched DNA amplification multimers for the sensitive, direct detection of human hepatitis viruses. Nucleic Acids Symp. Ser. 24: 197- 200
64. Velasco, J., M. T. Zarrabeitia, J. R. Prieto, J. L. Perez-Castrillon, M. D. Perez-Aguilar et al., 2010 Wnt pathway genes in osteoporosis and osteoarthritis: differential expression and genetic association study. Osteoporos. Int. 21: 109-118
65. Ward, B. D., B. D. Furman, J. L. Huebner, V. B. Kraus, F. Guilak et al., 2008 Absence of posttraumatic arthritis following intraarticular fracture in the MRL/MpJ mouse. Arthritis Rheum. 58: 744-753
66. Yan, Y., D. Tang, M. Chen, J. Huang, R. Xie et al., 2009 Axin2 controls bone remodeling through the beta-catenin-BMP signaling pathway in adult mice. J. Cell Sci. 122: 3566-3578
67. Yang, W., B. Maqsodi, Y. Ma, S. Bui, K. L. Crawford et al., 2006 Direct quantification of gene expression in homogenates of formalin-fixed, paraffin-embedded tissues. Biotechniques 40: 481-486
68. Yu, H. M., B. Jerchow, T. J. Sheu, B. Liu, F. Costantini et al., 2005 The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development 132: 1995-2005
69. Zhang, Z., J. L. Bryan, E. DeLassus, L.W. Chang,W. Liao et al., 2010 CCAAT/ Enhancer-binding protein {beta} and NF-{kappa}B mediate high level expression of chemokine genes CCL3 and CCL4 by human chondrocytes in response to IL-1{beta}. J. Biol. Chem. 285: 33092-33103
70. Zienolddiny, S.,D.Campa,H. Lind, D. Ryberg,V. Skaug et al., 2006 Polymorphisms of DNA repair genes and risk of non-small cell lung cancer. Carcinogenesis 27: 560-567