Nuclear DNA content variation associated with muscle fiber hypertrophic growth in fishes

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 182, Issue 4, 2012, Pages 531-540

  Jimenez, Ana Gabriela ^a   Kinsey, Stephen T ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Fish; Muscular endopolyploidy; Muscular hypertrophy; Nuclear DNA content

Indexed keywords

DNA;

ANIMAL; ARTICLE; ATLANTIC OCEAN; BLOOD; BODY SIZE; CELL NUCLEUS; CLASSIFICATION; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CYTOLOGY; DIPLOIDY; ERYTHROCYTE; FAST MUSCLE FIBER; FISH; GENETICS; HYPERTROPHY; METABOLISM; POLYPLOIDY; SPECIES DIFFERENCE; UNITED STATES;

ANIMALS; ATLANTIC OCEAN; BODY SIZE; CELL NUCLEUS; DIPLOIDY; DNA; ERYTHROCYTES; FISHES; HYPERTROPHY; MICROSCOPY, CONFOCAL; MUSCLE FIBERS, FAST-TWITCH; NORTH CAROLINA; POLYPLOIDY; SPECIES SPECIFICITY;

ANIMALIA; PISCES;

EID: 84859847417     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-011-0635-6     Document Type: Article

References (65)

1. Allen DL, Roy RR, Edgerton VR (1999) Myonuclear domains in muscle adaptation and disease. Musc Ner 22: 1350-1360 PMID: 10487900.
2. Beaton MJ, Hebert PDN (1999) Shifts in postembryonic somatic levels in Daphnia pulex. Hydrobiologia 394: 29-39. doi: 10. 1023/A: 1003567012950.
3. Bittner GD, Traut DL (1978) Growth of Crustacean muscles and muscle fibers. J Comp Physiol 124: 277-285. doi: 10. 1007/BF00657059.
4. Boudjelida H, Muntz L (1987) Multinucleation during myogenesis of the myotome of Xenopus laevis: a qualitative study. Development 101: 583-590.
5. Boyle KM, Dillaman RM, Kinsey ST (2003) Mitochondrial distribution and glycogen dynamics suggest diffusion constraints in muscle fibers of the blue crab, Callinectes sapidus. J Exp Zool 297A: 1-16. doi: 10. 1002/jez. a. 10227.
6. Bruusgaard JC, Liestøl K, Ekmark M, Kollstad K, Gundersen K (2003) Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J Physiol 551: 467-478. doi: 10. 1113/jphysiol. 2003. 045328.
7. Bruusgaard JC, Liestol K, Gunderson K (2006) Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged and old mice. J Appl Physiol 100: 2024-2030 PMID: 16497845.
8. Cardasis CA, Cooper GW (1975) An analysis of nuclear numbers in individual muscle fibers during differentiation and growth: a satellite cell-muscle fiber growth unit. J Exp Biol 191: 347-357. doi: 10. 1002/jez. 1401910305.
9. Champion DR (1984) The muscle satellite cell: a review. Int Rev Cyt 87: 225-251 PMID: 6370890.
10. Cheek DB (1985) The control of cell mass and replication. The DNA unit-a personal 20-year study. Early Hum Dev 12: 211-239 PMID: 3912156.
11. Coleman AW, Coder D, Goff LJ (1985) Polyploidy is the norm in the nuclei of cucurbit seedling. Plant Physiol 77: 39.
12. Comai L (2005) The advantages and disadvantages of being polyploidy. Nat Rev 6: 836-846. doi: 10. 1038/nrg1711.
13. Conlon I, Raff M (1999) Size control in animal development. Cell 96: 235-244. doi: 10. 1016/j. tig. 2007. 03. 005.
14. Dawley RM (1992) Clonal hybrids of the common laboratory fish Fundulus heteroclitus. PNAS 89: 2485-2488 PMID: 1549614.
15. Edgar BA, Orr-Weaver TL (2001) Endoreplication cell cycles: more for less. Cell 105: 297-306. doi: 10. 1016/S0092-8674(01)00334-8.
16. Flemming AJ, Shen Z-Z, Cunha A, Emmons SW, Leroi AM (2000) Somatic polyploidization and cellular proliferation drive body size evolution in nematodes. PNAS 97: 5285-5290 PMID: 10805788.
17. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR (1999) Ploidy regulation of gene expression. Science 285: 251-254. doi: 10. 1126/science. 285. 5425. 251.
18. Gold JR, Ragland CJ, Birkner MC, Garrett GP (1991) A simple procedure for long-term storage and preparation of fish cells for DNA content analysis using flow cytometry. Prog Fish Cultt 53: 108-110. doi: 10. 1577/15488640(1991)053<0108: TNASPF> 2. 3. CO; 2.
19. Gregory TR (2001) Coincidence, coevolution or causation? DNA content, cell size and the C-value enigma. Biol Rev 76: 65-101. doi: 10. 1111/j. 1469-185X. 2000. tb00059. x.
20. Gregory TR (2005) The c-value enigma in plants and animals: a review of parallels and an appeal for partnership. Ann Bot 95: 133-146. doi: 10. 1093/aob/mci009.
21. Gregory TR (2007) Animal Genome Size Database (online). Available from http://www. genomesize. com. Accessed 28 April 2011.
22. Hall ZW, Ralston E (1989) Nuclear domains in muscle cells. Cell 59: 771-772.
23. Hardie DC, Hebert PDN (2003) The nucleotypic effects of cellular DNA content in cartilaginous and ray-finned fishes. Genome 46: 683-706. doi: 10. 1139/g03-040.
24. Hardie DC, Hebert PDN (2004) Genome-size evolution in fishes. Can J Fish Aquat Sci 61: 1636-1646.
25. Hardy KM, Dillaman RM, Locke BR, Kinsey ST (2009) A skeletal muscle model of extreme hypertrophic growth reveals the influence of diffusion on cellular design. Am J Physiol Regul Integr Comp Physiol 296: R1855-R1867. doi: 10. 1152/ajpregu. 0076. 2009.
26. Hinegardner R (1968) Evolution of cellular DNA content in teleost fishes. Am Nat 102: 517-523.
27. Hinegardner R (1976) The cellular DNA content of sharks, rays and some other fishes. Comp Biochem Phys B 55: 367-370. doi: 10. 1016/0305-0491(76)90305-9.
28. Hinegardner R, Rosen DE (1972) Cellular DNA content and evolution of teleostean fishes. Am Nat 106: 621-644.
29. Jimenez AG, Locke BR, Kinsey ST (2008) The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans. J Exp Biol 211: 3214-3225. doi: 10. 1242/jeb. 020677.
30. Jimenez AG, Kinsey ST, Dillaman RM, Kapraun DF (2010) Nuclear DNA content variation associated with muscle fiber hypertrophic growth in decapod crustaceans. Genome 53: 161-171 PMID: 20237594.
31. Kapraun DF (2007) Nuclear DNA content estimates in green algal lineages: Chlorophyta and Streptophyta. Ann Bot 99: 677-701. doi: 10. 1093/aob/mcl294.
32. Kapraun DF, Dunwoody JT (2002) Relationship of nuclear genome size to some reproductive cell parameters in the Florideophycidae (Rhodophyta). Phycologia 41: 507-516.
33. Kapraun DF, Nguyen MN (1994) Karyology, nuclear DNA quantification and nucleus cytoplasmic domain variations in some multinucleate green algae. Phycologia 33: 42-52. doi: 10. 2216/i0031-8884-33-1-42. 1.
34. Kinsey ST, Hardy KM, Locke BR (2007) The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism of skeletal muscle. J Exp Biol 210: 3505-3512. doi: 10. 1242/jeb. 000331.
35. Kinsey ST, Locke BR, Dillaman RM (2011) Molecules in motion: influences of diffusion on metabolic structure and function in skeletal muscle. J Exp Biol 214: 263-274. doi: 10. 1242/jeb. 047985.
36. Koumans JT, Akster HA, Booms GHR, Lemmens CJJ, Osse JWM (1991) Numbers of myosatellite cells in white axial muscle of growing fish: Cyprinus carpio. Am J Anat 192: 418-424. doi: 10. 1002/aja. 1001920409.
37. Koumans JTM, Akster HA, Booms GHR, Osse JWM (1993) Growth of carp (Cyprinus carpio) white axial muscle; hyperplasia and hypertrophy in relation to the myonucleus/sarcoplasm ratio and the occurrence of different subclasses of myogenic cells. J Fish Biol 43: 69-80. doi: 10. 1111/j. 1095-8649. 1993. tb00411. x.
38. Koumans JTM, Akster HA, Witkam A, Osse JWM (1994) Numbers of muscle nuclei and myosatellite cell nuclei in red and white axial muscle during growth of the carp (Cyprinus carpio). J Fish Biol 44: 391-408. doi: 10. 1111/j. 1095-8649. 1994. tb01220. x.
39. Lozano E, Saez AG, Flemming AJ, Cunha A, Leroi AM (2006) Regulation of growth by ploidy in Caenorhabditis elegans. Curr Biol 16: 493-498. doi: 10. 1016/j. cub. 2006. 01. 048.
40. Luquet P, Durand G (1970) Évolution de la teneur en acides nucleiques de la musculature epaxiale au cours de la croissance chez la truite arc-en-ciel (Salmo Gairdnerii); roles respectifs de la multiplication et du grandissement cellulaires. Ann Biol Ani Biochim Biophys 10: 481-492.
41. Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from microorganisms. J Mol Biol 5: 109-118.
42. Matthew CA, Moore MJ (1987) Numbers of myonuclei and satellite cell nuclei in latissimus dorsi muscles of the chicken. Cell Tissue Res 248: 235-238. doi: 10. 1007/BF01239987.
43. Moss F, Leblond C (1970) Satellite cells as the source of nuclei in muscles of growing rats. J Cell Biol 44: 459-462. doi: 10. 1002/ar. 1091700405.
44. Netherlands S, Levitt LK, Robinson CS, Karpf ABC, Hodgson VRM, Wade RP, Hardeman EC (1998) Transcription occurs in pulses in muscle fibers. Genes Dev 12: 2748-2758. doi: 10. 1101/gad. 12. 17. 2748.
45. Nyack AC, Locke BR, Valenica A, Dillaman RM, Kinsey ST (2007) Scaling of post-contractile phosphocreatine recovery in fish white muscle: effect of intracellular diffusion. Am J Physiol 292: R1-R12. doi: 10. 1152/ajpregu. 00467. 20060363-6119/07.
46. Ojima Y, Yamamoto K (1990) Cellular DNA content of fishes determined by flow cytometry. La kromosoma II 57: 1871-1888.
47. Owens GK (1989) Control of hypertrophic versus hyperplastic growth of vascular smooth muscle cells. Am Phys Soc 257: H1755-H1765 PMID: 2690643.
48. Peterson DG, Stack SM, Healy JL, Donohoe BS, Anderson LK (1994) The relationship between synaptonemal complex length and genome size in four vertebrate classes (Osteichthyes, Reptilia, Aves, Mammalia). Chromosom Res 2: 153-162. doi: 10. 1007/BF01553494.
49. Pizon V, Gerbal F, Cifuentes Diaz C, Karsenti E (2005) Microtubule-dependent transport and organization of sarcomeric myosin during skeletal muscle differentiation. EMBO J 24: 3781-3792.
50. Portugal J, Waring MJ (1988) Assignment of DNA binding sites for 4′, 6-diamidine-2- phenylindole and bisbenzimide (Hoechst 33258). A comparative footprinting study. Biochim Biophis Acta 949: 158-168.
51. Priester C, Morton LC, Kinsey ST, Watanabe WO, Dillaman RM (2011) Growth patterns and nuclear distribution in white muscle fibers from black sea bass Centropristis striata (Linnaeus): evidence for the influence of diffusion. J Exp Biol 214: 1230-1239. doi: 10. 1242/jeb. 053199.
52. Ragland CJ, Gold JR (1989) Genome size variation in the North American sunfish genus Lepomis (Pisces: Centrarchidae). Genet Res 53: 173-182. doi: 10. 1017/S0016672300028135.
53. Schmalbruch H, Hellhammer U (1977) The number of nuclei in adult rat muscles with special reference to satellite cells. Anat Rec 189: 169-175. doi: 10. 1002/ar. 1091890204.
54. Scholz D, Baicu CF, Tuxworth WJ, Xu L, Kasiganesan H, Menick DR, Cooper G IV (2008) Microtubule dependent distribution of mRNA in adult cardiomyocytes. Am J Physiol Heart Circ Physiol 294: H1135-H1144.
55. Schwartz FJ, Maddock MB (1986) Comparisons of karyotypes and cellular DNA contents within and between major lines of elasmobranchs. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-Pacific fish biology. Ichthyological Society of Japan, Tokyo, pp 148-157.
56. Tiersch TR, Chandler RW, Kallman KD, Wachtel SS (1989) Estimation of nuclear DNA content by flow cytometry in fishes of the genus Xiphophorus. Comp Biochem Physiol 94B: 465-468. doi: 10. 1016/0305-0491(89)90182-X.
57. Traas J, Hülskamp M, Gendreau E, Höfte H (1998) Endoreduplication and development: rule without dividing? Curr Op Plant Biol 1: 498-503. doi: 10. 1016/S1369-5266(98)80042-3.
58. Valente LMP, Rocha E, Gomes EFS, Silva MW, Oliveira MH, Monteiro RAF, Fauconneau B (1999) Growth dynamics of white and red muscle fibers in fast- and slow-growing strains of rainbow trout. J Fish Biol 55: 675-691. doi: 10. 1111/j. 1095-8649. 1999. tb00710. x.
59. Vialli M (1957) Volume et contenu en ADN par noyau. Exp Cell Res Suppl 4: 284-293.
60. Vinogradov AE, Anatskaya OV, Kudryavtsev BN (2001) Relationship of hepatocyteploidy levels with body size and growth rate in mammals. Genome 44: 350-360. doi: 10. 1139/gen-44-3-350.
61. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia's fish species. Phil Trans Soc B 360: 1847-1857. doi: 10. 1098/rstb. 2005. 1716.
62. Weatherley AH, Gill HS (1985) Dynamics of size increase in muscle fibers in teleosts in relation to size and growth. Experientia 41: 353-354.
63. Weatherley A, Gill H (1987) Biology of fish growth. Academic press, San Diego.
64. Winick M, Noble A (1966) Cellular response in rats during malnutrition at various ages. J Nutr 89: 300-306 PMID: 5913937.
65. Wright CS (1984) Structural comparison of the two distinct sugar binding sites in wheat germ agglutinin isolectin II. J Mol Biol 178: 91-104 PMID: 6548265.