Decreased expression of adipose CD36 and FATP1 are associated with increased plasma non-esterified fatty acids during prolonged fasting in northern elephant seal pups (Mirounga angustirostris)

Journal of Experimental Biology

Volumn 215, Issue 14, 2012, Pages 2455-2464

  Viscarra, Jose Abraham ^a   Vázquez Medina, José Pablo ^a   Rodriguez, Ruben ^a   Champagne, Cory D ^b   Adams, Sean H ^c   Crocker, Daniel E ^d   Ortiz, Rudy M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SONOMA STATE UNIVERSITY   (United States)

Author keywords

Adipose tissue; Carnitine; Fasting; Insulin resistance; Lipid metabolism

Indexed keywords

ACYLCARNITINE; CARNITINE; CARNITINE PALMITOYLTRANSFERASE; CD36 ANTIGEN; DRUG DERIVATIVE; FATTY ACID; FATTY ACID TRANSPORTER; GLUCOSE; GLYCEROL; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); SIGNAL PEPTIDE; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE;

ADIPOSE TISSUE; ANIMAL; ARTICLE; BLOOD; BODY WEIGHT; DIET RESTRICTION; DRUG EFFECT; ENZYMOLOGY; LIPID METABOLISM; METABOLISM; NEWBORN; PHOCA; TIME; WESTERN BLOTTING;

ADIPOSE TISSUE; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD36; BLOTTING, WESTERN; BODY WEIGHT; CARNITINE; CARNITINE O-PALMITOYLTRANSFERASE; FASTING; FATTY ACID TRANSPORT PROTEINS; FATTY ACIDS, NONESTERIFIED; GLUCOSE; GLYCEROL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPASE; LIPID METABOLISM; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); SEALS, EARLESS; TIME FACTORS; TRIGLYCERIDES;

MAMMALIA; MIROUNGA ANGUSTIROSTRIS;

EID: 84863830184     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.069070     Document Type: Article

References (60)

1. Adams, S. H. (2011). Emerging perspectives on essential amino acid metabolism in obesity and the insulin-resistant state. Adv. Nutr. 2, 445-456.
2. Adams, S. H. and Costa, D. P. (1993). Water conservation and protein metabolism in northern elephant seal pups during the postweaning fast. J. Comp. Physiol. B 163, 367-373.
3. Adams, S. H., Costa, D. P. and Winter, S. C. (1992). Plasma carnitine in fasting neonatal and adult northern elephant seals. Am. J. Physiol. 263, E570-E574.
4. Adams, S. H., Hoppel, C. L., Lok, K. H., Zhao, L., Wong, S. W., Minkler, P. E., Hwang, D. H., Newman, J. W. and Garvey, W. T. (2009). Plasma acylcarnitine profiles suggest incomplete long-chain fatty acid b-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women. J. Nutr. 139, 1073-1081.
5. Alberts, A. W., Majerus, P. W., Talamo, B. and Vagelos, P. R. (1964). Acyl-carrier protein. II. Intermediary reactions of fatty acid synthesis. Biochemistry 3, 1563-1571.
6. Anthony, N. M., Gaidhu, M. P. and Ceddia, R. B. (2009). Regulation of visceral and subcutaneous adipocyte lipolysis by acute AICAR-induced AMPK activation. Obesity 17, 1312-1317.
7. Bertile, F. and Raclot, T. (2011). ATGL and HSL are not coordinately regulated in response to fuel partitioning in fasted rats. J. Nutr. Biochem. 22, 372-379.
8. Campbell, P. J., Carlson, M. G., Hill, J. O. and Nurjhan, N. (1992). Regulation of free fatty acid metabolism by insulin in humans: role of lipolysis and reesterification. Am. J. Physiol. 263, E1063-E1069. (Pubitemid 23024447)
9. Castellini, M. A., Costa, D. P. and Huntley, A. C. (1987). Fatty acid metabolism in fasting elephant seal pups. J. Comp. Physiol. B 157, 445-449.
10. Champagne, C. D., Houser, D. S. and Crocker, D. E. (2005). Glucose production and substrate cycle activity in a fasting adapted animal, the northern elephant seal. J. Exp. Biol. 208, 859-868. (Pubitemid 40428163)
11. Chaves, V. E., Frasson, D. and Kawashita, N. H. (2011). Several agents and pathways regulate lipolysis in adipocytes. Biochimie 93, 1631-1640.
12. Chen, X., Yu, Q. Q., Zhu, Y. H., Bi, Y., Sun, W. P., Liang, H., Cai, M. Y., He, X. Y. and Weng, J. P. (2010). Insulin therapy stimulates lipid synthesis and improves endocrine functions of adipocytes in dietary obese C57BL/6 mice. Acta Pharmacol. Sin. 31, 341-346.
13. Choi, S. M., Tucker, D. F., Gross, D. N., Easton, R. M., DiPilato, L. M., Dean, A. S., Monks, B. R. and Birnbaum, M. J. (2010). Insulin regulates adipocyte lipolysis via an Akt-independent signaling pathway. Mol. Cell. Biol. 30, 5009-5020.
14. Coburn, C. T., Knapp, F. F., Jr, Febbraio, M., Beets, A. L., Silverstein, R. L. and Abumrad, N. A. (2000). Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J. Biol. Chem. 275, 32523-32529.
15. Costa, D. P. and Ortiz, C. L. (1982). Blood chemistry homeostasis during prolonged fasting in the northern elephant seal. Am. J. Physiol. 242, R591-R595. (Pubitemid 12099163)
16. Doh, K.-O., Kim, Y.-W., Park, S.-Y., Lee, S.-K., Park, J. S. and Kim, J.-Y. (2005). Interrelation between long-chain fatty acid oxidation rate and carnitine palmitoyltransferase 1 activity with different isoforms in rat tissues. Life Sci. 77, 435-443. (Pubitemid 40719224)
17. Furler, S. M., Cooney, G. J., Hegarty, B. D., Lim-Fraser, M. Y., Kraegen, E. W. and Oakes, N. D. (2000). Local factors modulate tissue-specific NEFA utilization: assessment in rats using 3H-(R)-2-bromopalmitate. Diabetes 49, 1427-1433.
18. Gaidhu, M. P. and Ceddia, R. B. (2011). The role of adenosine monophosphate kinase in remodeling white adipose tissue metabolism. Exerc. Sport Sci. Rev. 39, 102-108.
19. Gaidhu, M. P., Anthony, N. M., Patel, P., Hawke, T. J. and Ceddia, R. B. (2010). Dysregulation of lipolysis and lipid metabolism in visceral and subcutaneous adipocytes by high-fat diet: role of ATGL, HSL, and AMPK. Am. J. Physiol. Cell Physiol. 298, C961-C971.
20. Gertow, K., Pietiläinen, K. H., Yki-Järvinen, H., Kaprio, J., Rissanen, A., Eriksson, P., Hamsten, A. and Fisher, R. M. (2004). Expression of fatty-Acid-handling proteins in human adipose tissue in relation to obesity and insulin resistance. Diabetologia 47, 1118-1125. (Pubitemid 38918172)
21. Golay, A., Swislocki, A. L. M., Chen, Y. D. and Reaven, G. M. (1987). Relationships between plasma-free fatty acid concentration, endogenous glucose production, and fasting hyperglycemia in normal and non-insulin-dependent diabetic individuals. Metabolism 36, 692-696. (Pubitemid 17100986)
22. Gruen, R., Kava, R. and Greenwood, M. R. C. (1980). Development of basal lipolysis and fat cell size in the epididymal fat pad of normal rats. Metabolism 29, 246-253. (Pubitemid 10129782)
23. Holland, R. and Hardie, D. G. (1985). Both insulin and epidermal growth factor stimulate fatty acid synthesis and increase phosphorylation of acetyl-CoA carboxylase and ATP-citrate lyase in isolated hepatocytes. FEBS Lett. 181, 308-312. (Pubitemid 15143929)
24. Horowitz, J. F., Mora-Rodriguez, R., Byerley, L. O. and Coyle, E. F. (1997). Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise. Am. J. Physiol. 273, E768-E775.
25. Houser, D. S., Champagne, C. D. and Crocker, D. E. (2007). Lipolysis and glycerol gluconeogenesis in simultaneously fasting and lactating northern elephant seals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R2376-R2381. (Pubitemid 350224032)
26. Iverson, S. J., Hamosh, M. and Bowen, W. D. (1995). Lipoprotein lipase activity and its relationship to high milk fat transfer during lactation in grey seals. J. Comp. Physiol. B 165, 384-395.
27. Kanatous, S. B., Hawke, T. J., Trumble, S. J., Pearson, L. E., Watson, R. R., Garry, D. J., Williams, T. M. and Davis, R. W. (2008). The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. J. Exp. Biol. 211, 2559-2565.
28. Karpe, F. and Tan, G. D. (2005). Adipose tissue function in the insulin-resistance syndrome. Biochem. Soc. Trans. 33, 1045-1048. (Pubitemid 41659110)
29. Knutson, V. P. (2000). The release of lipoprotein lipase from 3T3-L1 adipocytes is regulated by microvessel endothelial cells in an insulin-dependent manner. Endocrinology 141, 693-701. (Pubitemid 32250494)
30. Koves, T. R., Ussher, J. R., Noland, R. C., Slentz, D., Mosedale, M., Ilkayeva, O., Bain, J., Stevens, R., Dyck, J. R. B., Newgard, C. B. et al. (2008). Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 7, 45-56.
31. Leney, S. E. and Tavaré, J. M. (2009). The molecular basis of insulin-stimulated glucose uptake: signalling, trafficking and potential drug targets. J. Endocrinol. 203, 1-18.
32. McDonald, B. I. and Crocker, D. E. (2006). Physiology and behavior influence lactation efficiency in northern elephant seals (Mirounga angustirostris). Physiol. Biochem. Zool. 79, 484-496. (Pubitemid 43846265)
33. Mellish, J. E. and Loughlin, T. R. (2003). Lipoprotein lipase in lactating and neonatal northern fur seals: exploring physiological management of energetic conflicts. Comp. Biochem. Physiol. 134A, 147-156. (Pubitemid 36050858)
34. Mellish, J. E., Iverson, S. J., Bowen, W. D. and Hammill, M. O. (1999). Fat transfer and energetics during lactation in the hooded seal: the roles of tissue lipoprotein lipase in milk fat secretion and pup blubber deposition. J. Comp. Physiol. B 169, 377-390. (Pubitemid 29478284)
35. Minkler, P. E., Ingalls, S. T. and Hoppel, C. L. (2005). Strategy for the isolation, derivatization, chromatographic separation, and detection of carnitine and acylcarnitines. Anal. Chem. 77, 1448-1457. (Pubitemid 40327886)
36. Minkler, P. E., Stoll, M. S. K., Ingalls, S. T., Yang, S., Kerner, J. and Hoppel, C. L. (2008). Quantification of carnitine and acylcarnitines in biological matrices by HPLC electrospray ionization-mass spectrometry. Clin. Chem. 54, 1451-1462.
37. Naito, C. and Okada, K. (1975). Effect of glucose on lipolysis and on release of lipolytic products in isolated adipocytes. Am. J. Physiol. Leg. Content 228, 92-97.
38. Ong, J. M. and Kern, P. A. (1989). The role of glucose and glycosylation in the regulation of lipoprotein lipase synthesis and secretion in rat adipocytes. J. Biol. Chem. 264, 3177-3182. (Pubitemid 19063375)
39. Ortiz, C. L., Costa, D. P. and Le Boeuf, B. J. (1978). Water and energy flux in elephant seal pups fasting under natural conditions. Physiol. Zool. 51, 166-178.
40. Ortiz, C. L., Le Boeuf, B. J. and Costa, D. P. (1984). Milk intake of elephant seal pups: an index of parental investment. Am. Nat. 124, 416-422. (Pubitemid 16272500)
41. Ortiz, R. M., Wade, C. E. and Ortiz, C. L. (2001). Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R790-R795.
42. Ortiz, R. M., Wade, C. E. and Ortiz, C. L. (2003). Body water handling in response to hypertonic-saline induced diuresis in fasting northern elephant seal pups (Mirounga angustirostris). Comp. Biochem. Physiol. 134A, 423-428. (Pubitemid 36126575)
43. Patterson-Buckendahl, P., Adams, S. H., Morales, R., Jee, W. S. S., Cann, C. E. and Ortiz, C. L. (1994). Skeletal development in newborn and weanling northern elephant seals. Am. J. Physiol. Regul. Integr. Comp. Physiol. 267, R726-R734. (Pubitemid 24297586)
44. Perseghin, G., Petersen, K. and Shulman, G. I. (2003). Cellular mechanism of insulin resistance: potential links with inflammation. Int. J. Obes. Relat. Metab. Disord. 27 Suppl. 3, S6-S11. (Pubitemid 38019180)
45. Ramsay, R. R. and Zammit, V. A. (2004). Carnitine acyltransferases and their influence on CoA pools in health and disease. Mol. Aspects Med. 25, 475-493. (Pubitemid 39195072)
46. Rea, L. D. and Costa, D. P. (1992). Changes in standard metabolism during long-Term fasting in northern elephant seal pups (Mirounga angustirostris). Physiol. Zool. 65, 97-111.
47. Reiter, J., Stinson, N. L. and Boeuf, B. J. (1978). Northern elephant seal development: the transition from weaning to nutritional independence. Behav. Ecol. Sociobiol. 3, 337-367.
48. Reshef, L., Olswang, Y., Cassuto, H., Blum, B., Croniger, C. M., Kalhan, S. C., Tilghman, S. M. and Hanson, R. W. (2003). Glyceroneogenesis and the triglyceride/fatty acid cycle. J. Biol. Chem. 278, 30413-30416. (Pubitemid 36994541)
49. Riedman, M. and Ortiz, C. L. (1978). Changes in the milk composition during lactation in the northern elephant seal. Physiol. Zool. 52, 240-249.
50. Robinson, J. D., Bradley, R. M. and Brady, R. O. (1963). The utilization of substituted acyl-coenzyme a derivatives in fatty acid synthesis. II. Studies with enzymes obtained from adipose tissue. Biochemistry 2, 191-194.
51. Schwenk, R. W., Holloway, G. P., Luiken, J. J. F. P., Bonen, A. and Glatz, J. F. C. (2010). Fatty acid transport across the cell membrane: regulation by fatty acid transporters. Prostaglandins Leukot. Essent. Fatty Acids 82, 149-154.
52. Thorson, P. H. (1993). Development of diving in the northern elephant seal. PhD dissertation, University of California Santa Cruz.
53. Tift, M. S., Houser, D. S. and Crocker, D. E. (2011). High-density lipoprotein remains elevated despite reductions in total cholesterol in fasting adult male elephant seals (Mirounga angustirostris). Comp. Biochem. Physiol. 159B, 214-219.
54. Van Epps-Fung, M., Williford, J., Wells, A. and Hardy, R. W. (1997). Fatty acidinduced insulin resistance in adipocytes. Endocrinology 138, 4338-4345. (Pubitemid 27408479)
55. Vannier, C. and Ailhaud, G. (1989). Biosynthesis of lipoprotein lipase in cultured mouse adipocytes. II. Processing, subunit assembly, and intracellular transport. J. Biol. Chem. 264, 13206-13216. (Pubitemid 19194898)
56. Viscarra, J. A., Vázquez-Medina, J. P., Crocker, D. E. and Ortiz, R. M. (2011a). Glut4 is upregulated despite decreased insulin signaling during prolonged fasting in northern elephant seal pups. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R150-R154.
57. Viscarra, J. A., Champagne, C. D., Crocker, D. E. and Ortiz, R. M. (2011b). 5-AMPactivated protein kinase activity is increased in adipose tissue of northern elephant seal pups during prolonged fasting-induced insulin resistance. J. Endocrinol. 209, 317-325.
58. Wakil, S. J. (1961). Mechanism of fatty acid synthesis. J. Lipid Res. 2, 1-24.
59. Yue, P., Jin, H., Aillaud, M., Deng, A. C., Azuma, J., Asagami, T., Kundu, R. K., Reaven, G. M., Quertermous, T. and Tsao, P. S. (2010). Apelin is necessary for the maintenance of insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 298, E59-E67.
60. Yue, P., Jin, H., Xu, S., Aillaud, M., Deng, A. C., Azuma, J., Kundu, R. K., Reaven, G. M., Quertermous, T. and Tsao, P. S. (2011). Apelin decreases lipolysis via Gq, Gi, and AMPK-dependent mechanisms. Endocrinology 152, 59-68.