Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio)

Journal of Lipid Research

Volumn 50, Issue 8, 2009, Pages 1641-1652

  Flynn, Edward J ^a   Trent, Chad M ^a   Rawls, John F ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Adipocyte; Diet; Fish; In vivo imaging; Lipid droplet; Nile Red; Nutrition; Obesity; Pancreas; Preadipocyte

Indexed keywords

FAT DROPLET; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 11ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCLASSIFIED DRUG; FABP11 PROTEIN, ZEBRAFISH; FLUORESCENT DYE; LIPID; MESSENGER RNA; NILE RED; OXAZINE DERIVATIVE; ZEBRAFISH PROTEIN;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LINEAGE; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; GROWTH; IN SITU HYBRIDIZATION; IN VIVO STUDY; LARVAL STAGE; LIPID STORAGE; NONHUMAN; NUTRITION; ONTOGENY; PANCREAS; PRIORITY JOURNAL; PROADIPOCYTE; ZEBRA FISH; ANIMAL; ANIMAL MODEL; BODY COMPOSITION; BODY FAT DISTRIBUTION; BODY WEIGHT; FOOD; FOOD DEPRIVATION; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; HEMATOPOIETIC SYSTEM; HISTOLOGY; INTRAABDOMINAL FAT; METHODOLOGY; NUTRITIONAL STATUS; PHYSIOLOGY; PRENATAL DEVELOPMENT; ULTRASTRUCTURE; WHOLE BODY IMAGING;

ADIPOCYTES; ADIPOGENESIS; ANIMALS; BODY COMPOSITION; BODY FAT DISTRIBUTION; BODY WEIGHT; FATTY ACID-BINDING PROTEINS; FLUORESCENT DYES; FOOD; FOOD DEPRIVATION; GENE EXPRESSION; HEART; HEMATOPOIETIC SYSTEM; INTRA-ABDOMINAL FAT; LIPIDS; MODELS, ANIMAL; NUTRITIONAL STATUS; OXAZINES; PANCREAS; PPAR GAMMA; RNA, MESSENGER; WHOLE BODY IMAGING; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 69449086580     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800590-JLR200     Document Type: Article

References (63)

1. Department of Health and Human Services. (2001). The Surgeon General's Call to Action to Prevent and Decrease Overweight and Obesity. Public Health Service, Washington, DC.
2. Gesta, S., Y. H. Tseng, and C. R. Kahn. 2007. Developmental origin of fat: tracking obesity to its source. Cell. 131: 242-256.
3. Schlegel, A., and D. Y. Stainier. 2007. Lessons from "lower" organisms: what worms, flies, and zebrafish can teach us about human energy metabolism. PLoS Genet. 3: e199.
4. Fruhbeck, G., J. Gomez-Ambrosi, F. J. Muruzabal, and M. A. Burrell. 2001. The adipocyte: a model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am. J. Physiol. Endocrinol. Metab. 280: E827-E847.
5. Macia, L., O. Viltart, C. Verwaerde, M. Delacre, A. Delanoye, C. Grangette, and I. Wolowczuk. 2006. Genes involved in obesity: adipocytes, brain and microflora. Genes Nutr. 1: 189-212.
6. Billon, N., P. Iannarelli, M. C. Monteiro, C. Glavieux-Pardanaud, W. D. Richardson, N. Kessaris, C. Dani, and E. Dupin. 2007. The generation of adipocytes by the neural crest. Development. 134: 2283-2292.
7. Takashima, Y., T. Era, K. Nakao, S. Kondo, M. Kasuga, A. G. Smith, and S. Nishikawa. 2007. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell. 129: 1377-1388.
8. Pittenger, M. F., A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, J. D. Mosca, M. A. Moorman, D. W. Simonetti, S. Craig, and D. R. Marshak. 1999. Multilineage potential of adult human mesenchymal stem cells. Science. 284: 143-147.
9. Tang, W., D. Zeve, J. M. Suh, D. Bosnakovski, M. Kyba, R. E. Hammer, M. D. Tallquist, and J. M. Graff. 2008. White fat progenitor cells reside in the adipose vasculature. Science. 322: 583-586.
10. Zuk, P. A., M. Zhu, P. Ashjian, D. A. De Ugarte, J. I. Huang, H. Mizuno, Z. C. Alfonso, J. K. Fraser, P. Benhaim, and M. H. Hedrick. 2002. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell. 13: 4279-4295.
11. Rodeheffer, M. S., K. Birsoy, and J. M. Friedman. 2008. Identification of white adipocyte progenitor cells in vivo. Cell. 135: 240-249.
12. Hong, K. M., M. D. Burdick, R. J. Phillips, D. Heber, and R. M. Strieter. 2005. Characterization of human fibrocytes as circulating adipocyte progenitors and the formation of human adipose tissue in SCID mice. FASEB J. 19: 2029-2031.
13. Faust, I. M., P. R. Johnson, and J. Hirsch. 1980. Long-term effects of early nutritional experience on the development of obesity in the rat. J. Nutr. 110: 2027-2034.
14. Dugail, I., A. Quignard-Boulange, and F. Dupuy. 1986. Role of adipocyte precursors in the onset of obesity induced by overfeeding in suckling rats. J. Nutr. 116: 524-535.
15. Spalding, K. L., E. Arner, P. O. Westermark, S. Bernard, B. A. Buchholz, O. Bergmann, L. Blomqvist, J. Hoffstedt, E. Naslund, T. Britton, et al. 2008. Dynamics of fat cell turnover in humans. Nature. 453: 783-787.
16. Soukas, A., N. D. Socci, B. D. Saatkamp, S. Novelli, and J. M. Friedman. 2001. Distinct transcriptional profiles of adipogenesis in vivo and in vitro. J. Biol. Chem. 276: 34167-34174.
17. Billon, N., M. C. Monteiro, and C. Dani. 2008. Developmental origin of adipocytes: new insights into a pending question. Biol. Cell. 100: 563-575.
18. Patton, E. E., and L. I. Zon. 2001. The art and design of genetic screens: zebrafish. Nat. Rev. Genet. 2: 956-966.
19. Farber, S. A., M. Pack, S. Y. Ho, I. D. Johnson, D. S. Wagner, R. Dosch, M. C. Mullins, H. S. Hendrickson, E. K. Hendrickson, and M. E. Halpern. 2001. Genetic analysis of digestive physiology using fluorescent phospholipid reporters. Science. 292: 1385-1388.
20. Pickart, M. A., E. W. Klee, A. L. Nielsen, S. Sivasubbu, E. M. Mendenhall, B. R. Bill, E. Chen, C. E. Eckfeldt, M. Knowlton, M. E. Robu, et al. 2006. Genome-wide reverse genetics framework to identify novel functions of the vertebrate secretome. PLoS One. 1: e104.
21. Rawls, J. F., M. A. Mahowald, R. E. Ley, and J. I. Gordon. 2006. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 127: 423-433.
22. Schlegel, A., and D. Y. Stainier. 2006. Microsomal triglyceride transfer protein is required for yolk lipid utilization and absorption of dietary lipids in zebrafish larvae. Biochemistry. 45: 15179-15187.
23. Jones, K. S., A. P. Alimov, H. L. Rilo, R. J. Jandacek, L. A. Woollett, and W. T. Penberthy. 2008. A high throughput live transparent animal bioassay to identify non-toxic small molecules or genes that regulate vertebrate fat metabolism for obesity drug development. Nutr. Metab. (Lond). 5: 23.
24. Ibabe, A., E. Bilbao, and M. P. Cajaraville. 2005. Expression of peroxisome proliferator-activated receptors in zebrafish (Danio rerio) depending on gender and developmental stage. Histochem. Cell Biol. 123: 75-87.
25. Song, Y., and R. D. Cone. 2007. Creation of a genetic model of obesity in a teleost. FASEB J. 21: 2042-2049.
26. Om, A. D., T. Umino, H. Nakagawa, T. Sasaki, K. Okada, M. Asano, and A. Nakagawa. 2001. The effects of dietary EPA and DHA fortification on lipolysis activity and physiological function in juvenile black sea bream Acanthopagrus schlegeli (Bleeker). Aquac. Res. 32: 255-262.
27. Sheridan, M. A. 1988. Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp. Biochem. Physiol. B. 90: 679-690.
28. Albalat, A., A. Saera-Vila, E. Capilla, J. Gutierrez, J. Perez-Sanchez, and I. Navarro. 2007. Insulin regulation of lipoprotein lipase (LPL) activity and expression in gilthead sea bream (Sparus aurata). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 148: 151-159.
29. Company, R., J. Calduch-Giner, S. Kaushik, and J. Perez-Sanchez. 1999. Growth performance and adiposity in gilthead sea bream (Sparus aurata): risks and benefits of the high energy diets. Aquaculture. 171: 279-292.
30. Bellardi, S., M. L. Bianchini, L. Domenis, and G. B. Palmegiano. 1995. Effect of feeding schedule and feeding rate on size and number of adipocytes in rainbow trout Oncorhynchus mykiss. J. World Aquac. Soc. 26: 80-83.
31. Roy, S. S., M. Mukherjee, S. Bhattacharya, C. N. Mandal, L. R. Kumar, S. Dasgupta, I. Bandyopadhyay, and K. Wakabayashi. 2003. A new cell secreting insulin. Endocrinology. 144: 1585-1593.
32. Vegusdal, A., H. Sundvold, T. Gjoen, and B. Ruyter. 2003. An in vitro method for studying the proliferation and differentiation of Atlantic salmon preadipocytes. Lipids. 38: 289-296.
33. Oku, H., M. Tokuda, T. Okumura, and T. Umino. 2006. Effects of insulin, triiodothyronine and fat soluble vitamins on adipocyte differentiation and LPL gene expression in the stromal-vascular cells of red sea bream, Pagrus major. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 144: 326-333.
34. Oku, H., and T. Umino. 2008. Molecular characterization of peroxisome proliferator-activated receptors (PPARs) and their gene expression in the differentiating adipocytes of red sea bream Pagrus major. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 151: 268-277.
35. Albalat, A., J. Gutierrez, and I. Navarro. 2005. Regulation of lipolysis in isolated adipocytes of rainbow trout (Oncorhynchus mykiss): the role of insulin and glucagon. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 142: 347-354.
36. Westerfield, M. 2000. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). University of Oregon Press, Eugene, OR.
37. Kimmel, C. B., W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203: 253-310.
38. Russell, L., and S. Burguet. 1977. Ultrastructure of Leydig cells as revealed by secondary tissue treatment with a ferrocyanide:osmium mixture. Tissue Cell. 9: 751-766.
39. Reynolds, E. S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17: 208-212.
40. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497-509.
41. Elizondo, M. R., B. L. Arduini, J. Paulsen, E. L. MacDonald, J. L. Sabel, P. D. Henion, R. A. Cornell, and D. M. Parichy. 2005. Defective skeletogenesis with kidney stone formation in dwarf zebrafish mutant for trpm7. Curr. Biol. 15: 667-671.
42. Greenspan, P., and S. D. Fowler. 1985. Spectrofluorometric studies of the lipid probe, nile red. J. Lipid Res. 26: 781-789.
43. Field, H. A., P. D. Dong, D. Beis, and D. Y. Stainier. 2003. Formation of the digestive system in zebrafish. II. Pancreas morphogenesis. Dev. Biol. 261: 197-208.
44. Sadler, K. C., A. Amsterdam, C. Soroka, J. Boyer, and N. Hopkins. 2005. A genetic screen in zebrafish identifies the mutants vps18, nf2 and foie gras as models of liver disease. Development. 132: 3561-3572.
45. Napolitano, L. 1963. The differentiation of white adipose cells: an electron microscope study. J. Cell Biol. 18: 663-679.
46. Yanagiya, T., A. Tanabe, and K. Hotta. 2007. Gap-junctional communication is required for mitotic clonal expansion during adipogenesis. Obesity (Silver Spring). 15: 572-582.
47. Rosen, E. D., P. Sarraf, A. E. Troy, G. Bradwin, K. Moore, D. S. Milstone, B. M. Spiegelman, and R. M. Mortensen. 1999. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell. 4: 611-617.
48. Barak, Y., M. C. Nelson, E. S. Ong, Y. Z. Jones, P. Ruiz-Lozano, K. R. Chien, A. Koder, and R. M. Evans. 1999. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell. 4: 585-595.
49. Tontonoz, P., and B. M. Spiegelman. 2008. Fat and beyond: the diverse biology of PPAR gamma. Annu. Rev. Biochem. 77: 289-312.
50. Escriva, H., R. Safi, C. Hanni, M. C. Langlois, P. Saumitou-Laprade, D. Stehelin, A. Capron, R. Pierce, and V. Laudet. 1997. Ligand binding was acquired during evolution of nuclear receptors. Proc. Natl. Acad. Sci. USA. 94: 6803-6808.
51. Bertrand, S., B. Thisse, R. Tavares, L. Sachs, A. Chaumot, P. L. Bardet, H. Escriva, M. Duffraisse, O. Marchand, R. Safi, et al. 2007. Unexpected novel relational links uncovered by extensive developmental profiling of nuclear receptor expression. PLoS Genet. 3: e188.
52. Furuhashi, M., and G. S. Hotamisligil. 2008. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat. Rev. Drug Discov. 7: 489-503.
53. Hunt, C. R., J. H. Ro, D. E. Dobson, H. Y. Min, and B. M. Spiegelman. 1986. Adipocyte P2 gene: developmental expression and homology of 5′-flanking sequences among fat cell-specific genes. Proc. Natl. Acad. Sci. USA. 83: 3786-3790.
54. Makowski, L., J. B. Boord, K. Maeda, V. R. Babaev, K. T. Uysal, M. A. Morgan, R. A. Parker, J. Suttles, S. Fazio, G. S. Hotamisligil, et al. 2001. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat. Med. 7: 699-705.
55. Rolph, M. S., T. R. Young, B. O. Shum, C. Z. Gorgun, C. Schmitz-Peiffer, I. A. Ramshaw, G. S. Hotamisligil, and C. R. Mackay. 2006. Regulation of dendritic cell function and T cell priming by the fatty acid-binding protein AP2. J. Immunol. 177: 7794-7801.
56. Liu, R. Z., V. Saxena, M. K. Sharma, C. Thisse, B. Thisse, E. M. Denovan-Wright, and J. M. Wright. 2007. The fabp4 gene of zebrafish (Danio rerio) - genomic homology with the mammalian FABP4 and divergence from the zebrafish fabp3 in developmental expression. FEBS J. 274: 1621-1633.
57. Karanth, S., E. M. Denovan-Wright, C. Thisse, B. Thisse, and J. M. Wright. 2008. The evolutionary relationship between the duplicated copies of the zebrafish fabp11 gene and the tetrapod FABP4, FABP5, FABP8 and FABP9 genes. FEBS J. 275: 3031-3040.
58. Hotamisligil, G. S., R. S. Johnson, R. J. Distel, R. Ellis, V. E. Papaioannou, and B. M. Spiegelman. 1996. Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science. 274: 1377-1379.
59. Murayama, E., K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel. 2006. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity. 25: 963-975.
60. Umino, T., H. Nakagawa, and K. Arai. 1996. Development of adipose tissue in juvenile red sea bream. Fish. Sci. 62: 520-523.
61. Green, H., and O. Kehinde. 1975. An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell. 5: 19-27.
62. Bäckhed, F., H. Ding, T. Wang, L. V. Hooper, G. Y. Koh, A. Nagy, C. F. Semenkovich, and J. I. Gordon. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA. 101: 15718-15723.
63. Bäckhed, F., J. K. Manchester, C. F. Semenkovich, and J. I. Gordon. 2007. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl. Acad. Sci. USA. 104: 979-984.