Activation of Pax7-positive cells in a non-contractile tissue contributes to regeneration of myogenic tissues in the electric fish S. macrurus

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Weber, Christopher M ^a,d   Martindale, Mark Q ^b   Tapscott, Stephen J ^c   Unguez, Graciela A ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROLYTE; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTEMA; CELL ACTIVATION; CELL FUNCTION; CELL LINEAGE; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOLOGY; ELECTRIC FISH; IN VIVO STUDY; MOLECULAR WEIGHT; MUSCLE CELL; MUSCLE FIBER CONTRACTION; MUSCLE STEM CELL; MUSCLE TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SATELLITE CELL; SKELETAL MUSCLE; SPINAL CORD; STEM CELL; STERNOPYGUS MACRURUS; TISSUE REGENERATION; AMINO ACID SEQUENCE; ANIMAL; ELECTRIC ORGAN; GENETICS; METABOLISM; MOLECULAR GENETICS; MUSCLE CONTRACTION; PHYSIOLOGY; SEQUENCE HOMOLOGY;

AMPHIBIA; METAZOA; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; ELECTRIC FISH; ELECTRIC ORGAN; MOLECULAR SEQUENCE DATA; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; PAX7 TRANSCRIPTION FACTOR; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84861673299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036819     Document Type: Article

References (71)

1. Carlson BM, (2005) Some principles of regeneration in mammalian systems. Anat Rec 287B: 4-13.
2. van Bekkum DW, (2004) Phylogenetic aspects of tissue regeneration: role of stem cells. A concise overview Blood Cells Mol Dis 32: 11-6.
3. Fausto N, Riehle KJ, (2005) Mechanisms of liver regeneration and their clinical implications. J Hepatobiliary Pancreat Surg 12: 181-9.
4. Charge SB, Rudnicki MA, (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84: 209-38.
5. 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.
6. Brockes JP, Kumar A, (2002) Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat Rev Mol Cell Biol 3: 566-74.
7. Nye HL, Cameron JA, Chernoff EA, Stocum DL, (2003) Regeneration of the urodele limb: A review. Dev Dyn 226: 280-94.
8. Tsonis PA, (2000) Regeneration in vertebrates. Dev Biol 221: 273-284.
9. Morrison JI, Lööf S, He P, Simon A, (2006) Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J Cell Biol 172: 433-440.
10. Tanaka EM, Reddien PW, (2011) The cellular basis for animal regeneration. Dev Cell 21: 172-185.
11. Brockes JP, Kumar A, (2005) Appendage regeneration in adult vertebrates and implications for regenerative medicine. Science 310: 1919-1923.
12. Echeverri K, Tanaka EM, (2002) Mechanisms of muscle dedifferentiation during regeneration. Semin Cell Dev Biol 13: 353-60.
13. Stocum DL, (2004) Amphibian regeneration and stem cells. Curr Top Microbiol Immunol 280: 1-70.
14. Duckmanton A, Kumar A, Chang Y-T, Brockes JP, (2005) A single-cell analysis of myogenic dedifferentiation induced by small molecules. Chem Biol 12: 1117-1126.
15. Kumar A, Velloso CP, Imokawa Y, Brockes JP, (2000) Plasticity of retrovirus-labelled myotubes in the newt limb regeneration blastema. Dev Biol 218, 125-136.
16. Bennett MVL, (1971) Electric Organs. In: Hoar WS, Randall DJ, editors. Fish Physiology Academic Press pp. 347-491.
17. Baillet-Derbin, C, (1978) Cytodifferentiation of the regenerating electrocyte in an electric Fish. Biol Cell 33: 15-24.
18. Kirschbaum F, Meunier FJ, (1981) Experimental regeneration of the caudal skeletal of the glass knifefish Eigenmania virescens J Morphol 168: 121-135.
19. Kirschbaum F, Meunier FJ, (1988) South American gymnnotiform fishes as model animals for regeneration experiments. Monogr Dev Biol 21: 112-123.
20. Meunier FJ, Kirschbaum F, (1979) Comparative anatomy of the axial caudal skeleton of Gymnotoidei. Third European Ichthyological Congress, Warsaw.
21. Patterson JP, Zakon HH, (1993) Bromodeoxyuridine labeling reveals a class of satellite-like cells within the electric organ. J Neurobiol 24: 660-674.
22. Sîrbulescu RF, Ilies? I, Zupanc GK, (2009) Structural and functional regeneration after spinal cord injury in the weakly electric teleost fish, Apteronotus leptorhynchus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195: 699-714.
23. Zakon HH, (1991) Regeneration of electroreceptors in weakly electric fish. Ciba Found Symp 160: 294-308.
24. Anderson MJ, Waxman GG, (1981) Morphology of regenerated spinal cord in Sternarchus albifrons. Cell Tiss Res 219: 1-8.
25. Zakon HH, Unguez GA, (1999) Development and regeneration of the electric organ. J Exp Biol 202: 1427-1434.
26. Brusca RC, Brusca GJ, (1990) Invertebrates. Sunderland, Mass Sinauer Associates, Inc.
27. Alvarado AS, (2000) Regeneration in the metazoans: why does it happen?. BioEssays 22: 578-590.
28. Unguez GA, Zakon HH, (1998) Phenotypic conversion of distinct muscle fiber populations to electrocytes in a weakly electric fish. J Comp Neurol 399: 20-34.
29. Unguez GA, Zakon HH, (2002) Skeletal muscle transformation into electric organ in S. macrurus depends on innervation. J Neurobiol 53: 391-402.
30. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA, (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102: 777-786.
31. Kim JA, Laney C, Curry J, Unguez GA, (2008) Expression of Myogenic Regulatory Factors in the Muscle Derived Electric Organ of Sternopygus macrurus. J Exp Biol 211: 2172-2184.
32. Cuellar H, Kim JA, Unguez GA, (2006) Evidence of post-transcriptional regulation in the maintenance of a partial muscle phenotype by electrogenic cells of S. macrurus. FASEB J 20: E1856-E1865.
33. Kim JA, Jonsson CB, Calderone T, Unguez GA, (2004) Transcription of MyoD and myogenin in the non-contractile electrogenic cells of the weakly electric fish S. macrurus. Dev Genes Evo 214: 380-392.
34. Choi D, Li D, Raisman G, (2002) Fluorescent retrograde neuronal tracers that label the rat facial nucleus: a comparison of Fast Blue, Fluoro-ruby, Fluoro-emerald, Fluoro-gold and DiI. J Neurosci Methods 117: 167-172.
35. Shimotori T, Goto T, (2001) Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: relationship to protostomes. Dev Growth Differ 43: 371-82.
36. Bolte S, Corderlieres FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Micros 224: 213-232.
37. Seo HC, Saetre BO, Håvik B, Ellingsen S, Fjose A, (1998) The zebrafish Pax3 and Pax7 homologues are highly conserved, encode multiple isoforms and show dynamic segment-like expression in the developing brain. Mech Dev 70S: 49-63.
38. Ziman MR, Fletcher S, Kay PH, (1997) Alternate Pax7 transcripts are expressed specifically in skeletal muscle, brain and other organs of adult mice. Int J Biochem Cell Biol 29: 1029-36.
39. Jostes B, Walther C, Gruss P, (1990) The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system. Mech Dev 33: 27-37.
40. Schultz E, Chamberlain C, McCormick KM, Mozdziak PE, (2006) Satellite cells express distinct patterns of myogenic proteins in immature skeletal muscle. Dev Dyn 235: 3230-3239.
41. Ishido, Uda M, Kasuga M, Masuhara N, M, (2008) The expression patterns of Pax7 in satellite cells during overload-induced rat adult skeletal muscle hypertrophy. Acta Physiologica 195: 459-469.
42. Chen Y, Lin GF, Slack JMW, (2006) Control of muscle regeneration in the Xenopus tadpole tail by Pax7. Dev 133: 2303-2313.
43. Steinbacher P, Haslett JR, Obermayer A, Marschallinger J, Bauer HC, et al. (2007) MyoD and Myogenin Expression During Myogenic Phases in Brown Trout: A precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth. Dev Dyn 236: 1106-1114.
44. Halevy O, Piestun Y, Allouh MZ, Rosser BWC, Rinkevich Y, et al. (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231: 489-502.
45. McHedlishvili L, Epperlein HH, Telzerow A, Tanaka EM, (2007) A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors. Dev 134: 2083-2093.
46. Schnapp E, Tanaka EM, (2005) Quantitative evaluation of morpholino-mediated protein knockdown of GFP, MSX1, and PAX7 during tail regeneration in Ambystoma mexicanum. Dev Dyn 232: 162-70.
47. Kawakami A, Kimura-Kawakami M, Nomura T, Fujisawa H, (1997) Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech. Dev 66, 119-130.
48. Brockes JP, (1998) Progenitor cells for regeneration: dedifferentiation and immortaliasation. In: Ferretti P, Geraudie J, editors. Cellular and Molecular Basis of Regeneration; from Invertebrates to Humans John Wiley and Sons Limited pp. 63-77.
49. Echeverri K, Clarke JD, Tanaka EM, (2001) In vivo imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. Dev Biol 236: 151-64.
50. Lo DC, Allen F, Brockes JP, (1993) Reversal of muscle differentiation during urodele limb regeneration. Proc Natl Acad Sci 90: 7230-7234.
51. Kumar A, Velloso CP, Imokawa Y, Brockes JP, (2004) The regenerative plasticity of isolated urodele myofibers and its dependence on Msx1. PLoS Biol 2: E218.
52. Gotensparre SM, Andersson E, Wargelius A, Hansen T, Johnston IA, (2006) Insight into the complex genetic network of tetraploid Atlantic salmon (Salmo salar L.): description of multiple novel Pax-7 splice variants. Gene 373: 8-15.
53. Sibthorpe D, Sturlaugsdóttir R, Kristjansson BK, Thorarensen H, Skúlason S, Johnston IA, (2006) Characterisation and expression of the paired box protein 7 (Pax7) gene in polymorphic Arctic charr (Salvelinus alpinus). Comp Biochem Physiol B Biochem Mol Biol 145: 371-8.
54. Cornelison DD, Wold BJ, (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191: 270-83.
55. Hawke TJ, Garry DJ, (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91: 534-51.
56. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR, (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166: 347-357.
57. Mauro A, (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495.
58. Asakura A, Komaki M, Rudnicki M, (2001) Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 68: 245-253.
59. Singh NK, Chae HS, Hwang IH, Yoo IM, Ahn CN, et al. (2007) Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. J Anim Sci 85: 1126-1135.
60. Wada MR, Inagawa-Ogashiwa M, Shimizu S, Yasumoto S, Hashimoto N, (2002) Generation of different fates from multipotent muscle stem cells. Dev 129: 2987-95.
61. Redshaw Z, McOrist S, Loughna P, (2010) Muscle origin of porcine satellite cells affects in vitro differentiation potential. Cell Biochem Funct 28: 403-411.
62. Archer E, Escobedo N, Kim HJ, Gabillard J-C, Unguez GA, (2008) Differential potential of primary myogenic cells derived from adult muscle and electric organ of the gymnotiform S. macrurus. Abstract Viewer/Itinerary Planner. Society for Developmental Biology.
63. Shadd V, Archer E, Escobedo, N, Kim HJ, Unguez GA, (2009) Culture of Myogenic Cells Derived from Adult Myogenic Tissues and Regeneration Blastema of the Gymnotiform S. macrurus. Abstract Viewer/Itinerary Planner. Society for Developmental Biology.
64. Feldman JL, Stockdale FE, (1991) Skeletal muscle satellite cell diversity: satellite cells form fibres of different types in culture. Dev Biol 143: 320-334.
65. Rosenblatt JD, Parry DJ, Partridge TA, (1996) Phenotype of adult mouse muscle myoblasts reflects their fibre type of origin. Differentiation 60: 39-45.
66. Dusterhoft S, Pette D, (1993) Satellite cells from slow rat muscle express slow myosin under appropriate culture conditions. Differentiation 53: 25-33.
67. Bonavaud S, Agbulut O, Nizard R, D'honneur G, Mouly V, Butler-Browne G, (2001) A discrepancy resolved: human satellite cells are not preprogrammed to fast and slow lineages. Neuromuscular Disorders. 11: 747-752.
68. Morrison JI, Borg P, Simon A, (2010) Plasticity and recovery of skeletal muscle satellite cells during limb regeneration. FASEB J 24: 750-756.
69. Feldman JL, DiMario JX, Stockdale FE, (1993) Developmental appearance of adult myoblasts (satellite cells): studies of adult myoblasts in culture and adult myoblast transfer into embryonic avian limbs. Prog Clin Biol Res 383B: 563-74.
70. Gabillard JC, Sabin N, Paboeuf G, (2010) In vitro characterization of proliferation and differentiation of trout satellite cells. Cell Tissue Res 342: 471-7.
71. Nechiporuk A, Keating MT, (2002) A proliferation gradient between proximal and msxb-expressing distal blastema directs zebrafish fin regeneration. Dev 129: 2607-2617.