Differential effects of chronic hypoxia and feed restriction on the expression of leptin and its receptor, food intake regulation and the endocrine stress response in common carp

Journal of Experimental Biology

Volumn 215, Issue 13, 2012, Pages 2273-2282

  Bernier, Nicholas J ^a   Gorissen, Marnix ^b   Flik, Gert ^b  

^a UNIVERSITY OF GUELPH   (Canada)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Appetite; Hypoxia; Leptin; Metabolism; Stress

Indexed keywords

FISH PROTEIN; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; OXYGEN;

ANIMAL; ANOXIA; ARTICLE; CARP; EATING; FOOD INTAKE; GENE EXPRESSION REGULATION; GENETICS; HYPOPHYSIS; HYPOTHALAMUS; METABOLISM; PHYSIOLOGY;

ANIMALS; ANOXIA; APPETITE REGULATION; CARPS; EATING; FISH PROTEINS; GENE EXPRESSION REGULATION; HYPOTHALAMUS; LEPTIN; OXYGEN; PITUITARY GLAND; RECEPTORS, LEPTIN; RNA, MESSENGER;

CYPRINUS CARPIO;

EID: 84862870749     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.066183     Document Type: Article

References (69)

1. Aguilar, A. J., Conde-Sieira, M., Polakof, S., Miguez, J. M. and Soengas, J. L. (2010). Central leptin treatment modulates brain glucosensing function and peripheral energy metabolism of rainbow trout. Peptides 31, 1044-1054.
2. Ahima, R. S. and Antwi, D. A. (2008). Brain regulation of appetite and satiety. Endocrinol. Metab. Clin. North Am. 37, 811-823.
3. Ahima, R. S. and Flier, J. S. (2000). Leptin. Annu. Rev. Physiol. 62, 413-437.
4. Ambrosini, G., Nath, A. K., Sierra-Honigmann, M. R. and Flores-Riveros, J. (2002). Transcriptional activation of the human leptin gene in response to hypoxia. Involvement of hypoxia-inducible factor 1. J. Biol. Chem. 277, 34601-34609.
5. Anagnostoulis, S., Karayiannakis, A. J., Lambropoulou, M., Efthimiadou, A., Polychronidis, A. and Simopoulos, C. (2008). Human leptin induces angiogenesis in vivo. Cytokine 42, 353-357.
6. Anubhuti. and Arora, S. (2008). Leptin and its metabolic interactions: an update. Diabetes Obes. Metab. 10, 973-993.
7. Baze, M. M., Schlauch, K. and Hayes, J. P. (2010). Gene expression of the liver in response to chronic hypoxia. Physiol. Genom. 41, 275-288.
8. Bennett, B. D., Solar, G. P., Yuan, J. Q., Mathias, J., Thomas, G. R. and Matthews, W. (1996). A role for leptin and its cognate receptor in hematopoiesis. Curr. Biol. 6, 1170-1180. (Pubitemid 26368751)
9. Bergmeyer, H. U. (1985). Methods for Enzymatic Analysis, Vol. VI. New York: Academic Press.
10. Bernier, N. J. (2006). The corticotropin-releasing factor system as a mediator of the appetite-suppressing effects of stress in fish. Gen. Comp. Endocrinol. 146, 45-55. (Pubitemid 43248706)
11. Bernier, N. J. (2010). Food intake regulation and disorders. In Fish Diseases and Disorders, Vol. 2, Non-Infectious Disorders, 2nd edn (ed. J. Leatherhead and P. T. K. Woo), pp. 238-266. Wallingford: CABI Publishing.
12. Bernier, N. J. and Craig, P. M. (2005). CRF-related peptides contribute to stress response and regulation of appetite in hypoxic rainbow trout. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R982-R990. (Pubitemid 41397045)
13. Bernier, N. J. and Peter, R. E. (2001). Appetite-suppressing effects of urotensin I and corticotropin-releasing hormone in goldfish (Carassius auratus). Neuroendocrinol. 73, 248-260. (Pubitemid 32424519)
14. Bernier, N. J., Alderman, S. L. and Bristow, E. N. (2008). Heads or tails? Stressorspecific expression of corticotropin-releasing factor and urotensin I in the preoptic area and caudal neurosecretory system of rainbow trout. J. Endocrinol. 196, 637- 648. (Pubitemid 351425519)
15. Bernier, N. J., Flik, G. and Klaren, P. H. M. (2009). Regulation and contribution of the corticotropic, melanotropic and thyrotropic axes to the stress response in fishes. In Fish Neuroendocrinology, Fish Physiology, Vol. 28 (ed. N. J. Bernier, G. Van Der Kraak, A. P. Farrell and C. J. Brauner), pp. 235-311. Burlington, MA: Academic Press.
16. Boutilier, R. G., Dobson, G., Hoeger, U. and Randall, D. J. (1988). Acute exposure to graded levels of hypoxia in rainbow trout (Salmo gairdneri): metabolic and respiratory adaptations. Respir. Physiol. 71, 69-82.
17. Buentello, J. A., Gatlin, D. M. and Neill, W. H. (2000). Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 182, 339-352. (Pubitemid 30081133)
18. Cao, Y.-B., Xue, J. L., Wu, L.-Y., Jiang, W., Hu, P.-N. and Zhu, J. (2011). The detection of 3 leptin receptor isoforms in crucian carp gill and the influence of fasting and hypoxia in their expression. Dom. Anim. Endocrinol. 41, 74-80.
19. Chabot, D. and Dutil, J. D. (1999). Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J. Fish Biol. 55, 472-491. (Pubitemid 29423048)
20. Chu, D. L., Li, V. W. and Yu, R. M. (2010). Leptin: clue to poor appetite in oxygenstarved fish. Mol. Cell. Endocrinol. 319, 143-146.
21. Copeland, D. L., Duff, R. J., Liu, Q., Prokop, J. and Londraville, R. L. (2011). Leptin in teleost fishes: an argument for comparative study. Front. Physiol. 2, 26.
22. Dangre, A. J., Manning, S. and Brouwer, M. (2010). Effects of cadmium on hypoxiainduced expression of hemoglobin and erythropoietin in larval sheepshead minnow, Cyprinodon variegatus. Aquat. Toxicol. 99, 168-175.
23. De Pedro, N., Martinez-Alvarez, R. and Delgado, M. J. (2006). Acute and chronic leptin reduces food intake and body weight in goldfish (Carassius auratus). J. Endocrinol. 188, 513-520.
24. Denver, R. J., Bonnett, R. M. and Boorse, G. C. (2011). Evolution of leptin structure and function. Neurodocrinol. 94, 21-38.
25. Diaz, R. J. and Brietburg, D. L. (2009). The hypoxic environment. In Hypoxia, Fish Physiology, Vol. 27 (ed. J. G. Richards, A. P. Farrell and C. J. Brauner), pp. 1-23. Burlington, MA: Academic Press.
26. Gallaugher, P. and Farrell, A. P. (1998). Hematocrit and blood oxygen-carrying capacity. In Fish Respiration, Fish Physiology, Vol. 17 (ed. S. F. Perry and B. L. Tufts), pp. 185-227. Burlington, MA: Academic Press.
27. Gingerich, A. J., Philipp, D. P. and Suski, C. D. (2010). Effects of nutritional status on metabolic rate, exercise and recovery in a freshwater fish. J. Comp. Physiol. B 180, 371-384.
28. Gorissen, M., Bernier, N. J., Nabuurs, S. B., Flik, G. and Huising, M. O. (2009). Two divergent leptin paralogues in zebrafish (Danio rerio) that originate early in teleostean evolution. J. Endocrinol. 201, 329-339.
29. Gorissen, M., Flik, G. and Huising, M. O. (2006). Peptides and proteins regulating food intake: a comparative view. Anim. Biol. 56, 447-473. (Pubitemid 44883991)
30. Gorissen, M., Bernier, N. J., Manuel, R., de Gelder, S., Metz, J. R., Huising, M. O. and Flik, G. (2012). Recombinant human leptin attenuates stress axis activity in common carp (Cyprinus carpio L.). Gen. Comp. Endocrinol. 178, 75-81.
31. Grosfeld, A., Andre, J., Hauguel-De Mouzon, S., Berra, E., Pouyssegur, J. and Guerre-Millo, M. (2002). Hypoxia-inducible factor 1 transactivates the human leptin gene promoter. J. Biol. Chem. 277, 42953-42957. (Pubitemid 35285673)
32. Guo, K., McMinn, J. E., Ludwig, T., Yu, Y., Yang, G., Chen, L., Loh, D., Li, C., Chua, S. and Zhang, Y. (2007). Disruption of peripheral leptin signaling in mice results in hyperleptinemia without associated metabolic abnormalities. Endocrinol. 148, 3987-3997. (Pubitemid 47105835)
33. Harrison, J. F. and Haddad, G. G. (2010). Effects of oxygen on growth and size: synthesis of molecular, organismal, and evolutionary studies with Drosophila melanogaster. Annu. Rev. Physiol. 73, 95-113.
34. Huising, M. O., Geven, E. J. W., Kruiswijk, C. P., Nabuurs, S. B., Stolte, E. H., Spanings, F. A. T., Verburg-van Kemenade, B. M. L. and Flik, G. (2006). Increased leptin expression in common carp (Cyprinus carpio) after food intake but not after fasting or feeding to satiation. Endocrinology 147, 5786-5797. (Pubitemid 44833495)
35. Johnson, A. B., Denko, N. and Barton, M. C. (2008). Hypoxia induces a novel signature of chromatin modifications and global repression of transcription. Mutat. Res. 640, 174-179.
36. Kelley, K. M., Haigwood, J. T., Perez, M. and Galima, M. M. (2001). Serum insulinlike growth factor binding proteins (IGFBPs) as markers for anabolic/catabolic condition in fishes. Comp. Biochem. Physiol. 129B, 229-236. (Pubitemid 32523943)
37. Kling, P., Rønnestad, I., Stefansson, S. O., Murashita, K., Kurokawa, T. and Björnsson, B. T. (2009). A homologous salmonid leptin radioimmunoassay indicates elevated plasma leptin levels during fasting of rainbow trout. Gen. Comp. Endocrinol. 162, 307-312.
38. Kurokawa, T., Uji, S. and Suzuki, T. (2005). Identification of cDNA coding for a homologue to mammalian leptin from pufferfish, Takifugu rubripes. Peptides 26, 745- 750. (Pubitemid 40461655)
39. Lai, J. C., Kakuta, I., Mok, H. O., Rummer, J. L. and Randall, D. (2006). Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen. J. Exp. Biol. 209, 2734-2738. (Pubitemid 44213119)
40. Li, G. G., Liang, X. F., Xie, Q., Li, G., Yu, Y. and Lai, K. (2010). Gene structure, recombinant expression and functional characterization of grass carp leptin. Gen. Comp. Endocrinol. 166, 117-127.
41. Londraville, R. L. and Duvall, C. S. (2002). Murine leptin injections increase intracellular fatty acid-binding protein in green sunfish (Lepomis cyanellus). Gen. Comp. Endocrinol. 129, 56-62. (Pubitemid 35333783)
42. Matsuda, K. (2009). Recent advances in the regulation of feeding behavior by neuropeptides in fish. Trends Comp. Endocrinol. Neurobiol. 1163, 241-250.
43. Metz, J. R., Geven, E. J. W., van den Burg, E. H. and Flik, G. (2005). ACTH, alpha- MSH, and control of cortisol release: cloning, sequencing, and functional expression of the melanocortin-2 and melanocortin-5 receptor in Cyprinus carpio. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R814-R826. (Pubitemid 41208448)
44. Murashita, K., Uji, S., Yamamoto, T., Rønnestad, I. and Kurokawa, T. (2008). Production of recombinant leptin and its effects on food intake in rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. 150B, 377-384.
45. Murashita, K., Jordal, A. E., Nilsen, T. O., Stefansson, S. O., Kurokawa, T., Björnsson, B. T., Moen, A. G. and Rønnestad, I. (2011). Leptin reduces Atlantic salmon growth through the central pro-opiomelanocortin pathway. Comp. Biochem. Physiol. 158A, 79-86.
46. Myers, M. G., Cowley, M. A. and Munzberg, H. (2008). Mechanisms of leptin action and leptin resistance. Annu. Rev. Physiol. 70, 537-556. (Pubitemid 351738191)
47. Nikinmaa, M. and Rees, B. B. (2005). Oxygen-dependent gene expression in fishes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1079-R1090. (Pubitemid 40593687)
48. Pedersen, C. L. (1987). Energy budgets for juvenile rainbow trout at various oxygen concentrations. Aquaculture 62, 289-298.
49. Peterson, B. C. and Small, B. C. (2004). Effects of fasting on circulating IGF-binding proteins, glucose, and cortisol in channel catfish (Ictalurus punctatus). Dom. Anim. Endocrinol. 26, 231-240. (Pubitemid 38285647)
50. Pichavant, K., Person-Le-Ruyet, J., Le Bayon, N., Severe, A., Le Roux, A. and Boeuf, G. (2001). Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. J. Fish Biol. 59, 875- 883. (Pubitemid 33136601)
51. Quintero, P., Milagro, F. I., Campion, J. and Martinez, J. A. (2010). Impact of oxygen availability on body weight management. Med. Hypotheses 74, 901-907.
52. Reidy, S. P. and Weber, J. (2000). Leptin: an essential regulator of lipid metabolism. Comp. Biochem. Physiol. 125A, 285-298. (Pubitemid 30224797)
53. Richards, J. G. (2009). Metabolic and molecular responses of fish to hypoxia. In Hypoxia, Fish Physiology, Vol. 27 (ed. J. G. Richards, A. P. Farrell and C. J. Brauner), pp. 443-485. Burlington, MA: Academic Press.
54. Ripley, J. L. and Foran, C. M. (2007). Influence of estuarine hypoxia on feeding and sound production by two sympatric pipefish species (Syngnathidae). Mar. Environ. Res. 63, 350-367. (Pubitemid 46282922)
55. Rønnestad, I., Nilsen, T. O., Murashita, K., Angotzi, A. R., Gamst Moen, A. G., Stefansson, S. O., Kling, P., Björnsson, B. T. and Kurokawa, T. (2010). Leptin and leptin receptor genes in Atlantic salmon: cloning, phylogeny, tissue distribution and expression correlated to long-term feeding status. Gen. Comp. Endocrinol. 168, 55-70.
56. Seasholtz, A. F., Valverde, R. A. and Denver, R. J. (2002). Corticotropin-releasing hormone-binding protein: biochemistry and function from fishes to mammals. J. Endocrinol. 175, 89-97. (Pubitemid 35276589)
57. Stockmann, C. and Fandrey, J. (2006). Hypoxia-induced erythropoietin production: a paradigm for oxygen-regulated gene expression. Clin. Exp. Pharmacol. Physiol. 33, 968-979. (Pubitemid 44429878)
58. Taglialatela, R. and Della Corte, F. (1997). Human and recombinant erythropoietin stimulate erythropoiesis in the goldfish Carassius auratus. Eur. J. Histochem. 41, 301-304. (Pubitemid 28059227)
59. Trayhurn, P., Thomas, M. E., Duncan, J. S. and Rayner, D. V. (1995). Effects of fasting and refeeding on ob gene expression in white adipose tissue of lean and obese (ob/ob) mice. FEBS Lett. 368, 488-490.
60. Ultsch, G. (1989). Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biol. Rev. 64, 435-516.
61. Van Raaij, M. T. M., VandenThillart, G. E. E. J. M., Vianen, G. J., Pit, D. S. S., Balm, P. H. M. and Steffens, B. (1996). Substrate mobilization and hormonal changes in rainbow trout (Oncorhynchus mykiss, L.) and common carp (Cyprinus carpio, L.) during deep hypoxia and subsequent recovery. J. Comp. Physiol. B 166, 443-452. (Pubitemid 27012480)
62. Volkoff, H., Eykelbosh, A. J. and Peter, R. E. (2003). Role of leptin in the control of feeding of goldfish Carassius auratus: interactions with cholecystokinin, neuropeptide Y and orexin A, and modulation by fasting. Brain Res. 972, 90-109. (Pubitemid 36507081)
63. Volkoff, H., Unniappan, S. and Kelly, S. P. (2009). The endocrine regulation of food intake. In Fish Neuroendocrinology, Fish Physiology, Vol. 28 (ed. N. J. Bernier, G. Van Der Kraak, A. P. Farrell and C. J. Brauner), pp. 421-465. Burlington, MA: Academic Press.
64. Wang, T., Hung, C. C. Y. and Randall, D. J. (2006). The comparative physiology of food deprivation: from feast to famine. Annu. Rev. Physiol. 68, 223-251.
65. Wang, T., Lefevre, S., Huang, D. T. T., Cong, N. V. and Bayley, M. (2009). The effects of hypoxia on growth and digestion. In Hypoxia, Fish Physiology, Vol. 27 (ed. J. G. Richards, A. P. Farrell and C. J. Brauner), pp. 361-396. Burlington, MA: Academic Press.
66. Wong, M. M., Yu, R. M., Ng, P. K., Law, S. H., Tsang, A. K. and Kong, R. Y. (2007). Characterization of a hypoxia-responsive leptin receptor (omLepR(L)) cDNA from the marine medaka (Oryzias melastigma). Mar. Pollut. Bull. 54, 797-803. (Pubitemid 46843119)
67. Yaqoob, N., Holotta, M., Prem, C., Kopp, R. and Schwerte, T. (2009). Ontogenetic development of erythropoiesis can be studied non-invasively in GATA-1:DsRed transgenic zebrafish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 154, 270-278.
68. Zhou, B. S., Wu, R. S. S., Randall, D. J., Lam, P. K. S., Ip, Y. K. and Chew, S. F. (2000). Metabolic adjustments in the common carp during prolonged hypoxia. J. Fish Biol. 57, 1160-1171.
69. Zhou, B. S., Wu, R. S. S., Randall, D. J. and Lam, P. K. S. (2001). Bioenergetics and RNA/DNA ratios in the common carp (Cyprinus carpio) under hypoxia. J. Comp. Physiol. B 171, 49-57. (Pubitemid 32161022)