Effect of chronic intermittent hypoxia on triglyceride uptake in different tissues

Journal of Lipid Research

Volumn 54, Issue 4, 2013, Pages 1058-1065

  Yao, Qiaoling ^a   Shin, Mi Kyung ^a   Jun, Jonathan C ^a   Hernandez, Karen L ^b   Aggarwal, Neil R ^a   Mock, Jason R ^a   Gay, Jason ^c   Drager, Luciano F ^d   Polotsky, Vsevolod Y ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Miami College of Engineering   (United States)

^c LEXICON PHARMACEUTICALS INC   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Angiopoietin like protein 4; Brown adipose tissue; Lipoprotein clearance; Lipoprotein lipase; Lungs; Obstructive sleep apnea; Pulmonary microvascular endothelial cells; White adipose tissue

Indexed keywords

ANGIOPOIETIN LIKE PROTEIN 4 NEUTRALIZING ANTIBODY; CD11B ANTIGEN; CD146 ANTIGEN; CD36 ANTIGEN; LIPID; LIPOPROTEIN LIPASE; NEUTRALIZING ANTIBODY; TRIACYLGLYCEROL; TRIOLEIN; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BROWN ADIPOSE TISSUE; CELL POPULATION; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVITY; ENZYME METABOLISM; HEART; LIPID TRANSPORT; LIVER; LPL GENE; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPLEEN; TREATMENT DURATION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANGIOPOIETINS; ANIMALS; ANOXIA; LIPOPROTEIN LIPASE; LIPOPROTEINS; LUNG; MALE; MICE; MICE, INBRED C57BL; TRIGLYCERIDES;

EID: 84875867755     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M034272     Document Type: Article

References (72)

1. Gastaut, H., C. A. Tassinari, and B. Duron. 1966. Polygraphic study of the episodic diurnal and nocturnal (hypnic and respiratory) manifestations of the Pickwick syndrome. Brain Res. 1 : 167-186.
2. Marshall, N. S., K. K. Wong, P. Y. Liu, S. R. Cullen, M. W. Knuiman, and R. R. Grunstein. 2008. Sleep apnea as an independent risk factor for all-cause mortality: the Busselton Health Study. Sleep. 31 : 1079-1085.
3. Young, T., L. Finn, P. E. Peppard, M. Szklo-Coxe, D. Austin, F. J. Nieto, R. Stubbs, and K. M. Hla. 2008. Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort. Sleep. 31 : 1071-1078.
4. Punjabi, N. M., B. S. Caffo, J. L. Goodwin, D. J. Gottlieb, A. B. Newman, G. T. O'Connor, D. M. Rapoport, S. Redline, H. E. Resnick, J. A. Robbins, et al. 2009. Sleep-disordered breathing and mortality: a prospective cohort study. PLoS Med. 6 : e1000132.
5. Drager, L. F., L. A. Bortolotto, M. C. Lorenzi, A. C. Figueiredo, E. M. Krieger, and G. Lorenzi-Filho. 2005. Early signs of atherosclerosis in obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 172 : 613-618.
6. Drager, L. F., L. A. Bortolotto, A. C. Figueiredo, E. M. Krieger, and G. Lorenzi-Filho. 2007. Effects of CPAP on early signs of atherosclerosis in obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 176 : 706-712.
7. Drager, L. F., J. Jun, and V. Y. Polotsky. 2010. Obstructive sleep apnea and dyslipidemia: implications for atherosclerosis. Curr. Opin. Endocrinol. Diabetes Obes. 17 : 161-165.
8. Drager, L. F., V. Y. Polotsky, and G. Lorenzi-Filho. 2011. Obstructive sleep apnea: an emerging risk factor for atherosclerosis. Chest. 140 : 534-542.
9. Chung, S., I. Y. Yoon, C. H. Lee, and J. W. Kim. 2010. The association of nocturnal hypoxemia with arterial stiffness and endothelial dysfunction in male patients with obstructive sleep apnea syndrome. Respiration. 79 : 363-369.
10. Newman, A. B., F. J. Nieto, U. Guidry, B. K. Lind, S. Redline, T. G. Pickering, and S. F. Quan. 2001. Relation of sleep-disordered breathing to cardiovascular disease risk factors: the Sleep Heart Health Study. Am. J. Epidemiol. 154 : 50-59.
11. Robinson, G. V., J. C. Pepperell, H. C. Segal, R. J. Davies, and J. R. Stradling. 2004. Circulating cardiovascular risk factors in obstructive sleep apnoea: data from randomised controlled trials. Thorax. 59 : 777-782.
12. Sharma, S. K., S. Agrawal, D. Damodaran, V. Sreenivas, T. Kadhiravan, R. Lakshmy, P. Jagia, and A. Kumar. 2011. CPAP for the metabolic syndrome in patients with obstructive sleep apnea. N. Engl. J. Med. 365 : 2277-2286.
13. Phillips, C. L., B. J. Yee, N. S. Marshall, P. Y. Liu, D. R. Sullivan, and R. R. Grunstein. 2011. Continuous positive airway pressure reduces postprandial lipidemia in obstructive sleep apnea: a randomized, placebo-controlled crossover trial. Am. J. Respir. Crit. Care Med. 184 : 355-361.
14. National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). 2002. Third report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) fi nal report. Circulation. 106: 3143-3421.
15. Freiberg, J. J., A. Tybjaerg-Hansen, J. S. Jensen, and B. G. Nordestgaard. 2008. Nonfasting triglycerides and risk of ischemic stroke in the general population. JAMA. 300 : 2142-2152.
16. Nordestgaard, B. G., M. Benn, P. Schnohr, and A. Tybjaerg-Hansen. 2007. Nonfasting triglycerides and risk of myocardial infarction, ischemic heart disease, and death in men and women. JAMA. 298 : 299-308.
17. Sposito, A. C., L. I. Ventura, C. G. Vinagre, P. A. Lemos, E. Quintella, R. D. Santos, O. Carneiro, J. A. Ramires, and R. C. Maranhao. 2004. Delayed intravascular catabolism of chylomicron-like emulsions is an independent predictor of coronary artery disease. Atherosclerosis. 176 : 397-403.
18. Vine, D. F., D. R. Glimm, and S. D. Proctor. 2008. Intestinal lipid transport and chylomicron production: possible links to exacerbated atherogenesis in a rodent model of the metabolic syndrome. Atheroscler. Suppl. 9 : 69-76.
19. Botham, K. M., and C. P. Wheeler-Jones. 2007. Introduction to the Biochemical Society Focused Meeting on Diet and Cardiovascular Health: chylomicron remnants and their emerging roles in vascular dysfunction in atherosclerosis. Biochem. Soc. Trans. 35 : 437-439.
20. Mahley, R. W., and Y. Huang. 2007. Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing. J. Clin. Invest. 117 : 94-98.
21. Jun, J., C. Reinke, D. Bedja, D. Berkowitz, S. Bevans-Fonti, J. Li, L. A. Barouch, K. Gabrielson, and V. Y. Polotsky. 2010. Effect of intermittent hypoxia on atherosclerosis in apolipoprotein E-defi cient mice. Atherosclerosis. 209 : 381-386.
22. Polotsky, V. Y., A. E. Rubin, A. Balbir, T. Dean, P. L. Smith, A. R. Schwartz, and C. P. O'Donnell. 2006. Intermittent hypoxia causes REM sleep defi cits and decreases EEG delta power in NREM sleep in the C57BL/6J mouse. Sleep Med. 7 : 7-16.
23. Savransky, V., S. Bevans, A. Nanayakkara, J. Li, P. L. Smith, M. S. Torbenson, and V. Y. Polotsky. 2007. Chronic intermittent hypoxia causes hepatitis in a mouse model of diet-induced fatty liver. Am. J. Physiol. Gastrointest. Liver Physiol. 293 : G871-G877.
24. Drager, L. F., J. Li, M. K. Shin, C. Reinke, N. R. Aggarwal, J. C. Jun, S. Bevans-Fonti, C. Sztalryd, S. M. O'Byrne, O. Kroupa, et al. 2012. Intermittent hypoxia inhibits clearance of triglyceride-rich lipoproteins and inactivates adipose lipoprotein lipase in a mouse model of sleep apnoea. Eur. Heart J. 33 : 783-790.
25. National Research Council. 2010. Guide for the Care and Use of Laboratory Animals. 8 th edition. National Academies Press, Washington, D.C.
26. Reinke, C., S. Bevans-Fonti, D. N. Grigoryev, L. F. Drager, A. C. Myers, R. A. Wise, A. R. Schwartz, W. Mitzner, and V. Y. Polotsky. 2011. Effects of different acute hypoxic regimens on tissue oxygen profi les and metabolic outcomes. Am. J. Physiol. Lung Cell. Mol. Physiol. 300 : L266-L273.
27. Desai, U., E. C. Lee, K. Chung, C. Gao, J. Gay, B. Key, G. Hansen, D. Machajewski, K. A. Platt, A. T. Sands, et al. 2007. Lipid-lowering effects of anti-Angiopoietin-like 4 antibody recapitulate the lipid phenotype found in angiopoietin-like 4 knockout mice. Proc. Natl. Acad. Sci. USA. 104 : 11766-11771.
28. van Bennekum, A. M., Y. Kako, P. H. Weinstock, E. H. Harrison, R. J. Deckelbaum, I. J. Goldberg, and W. S. Blaner. 1999. Lipoprotein lipase expression level infl uences tissue clearance of chylomicron retinyl ester. J. Lipid Res. 40 : 565-574.
29. Augustus, A. S., Y. Kako, H. Yagyu, and I. J. Goldberg. 2003. Routes of FA delivery to cardiac muscle: modulation of lipoprotein lipolysis alters uptake of TG-derived FA. Am. J. Physiol. Endocrinol. Metab. 284 : E331-E339.
30. Nilsson-Ehle, P., and M. C. Schotz. 1976. A stable, radioactive substrate emulsion for assay of lipoprotein lipase. J. Lipid Res. 17 : 536-541.
31. Li, J., L. N. Thorne, N. M. Punjabi, C. K. Sun, A. R. Schwartz, P. L. Smith, R. L. Marino, A. Rodriguez, W. C. Hubbard, C. P. O'Donnell, et al. 2005. Intermittent hypoxia induces hyperlipidemia in lean mice. Circ. Res. 97 : 698-706.
32. Schmittgen, T. D., and K. J. Livak. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3 : 1101-1108.
33. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25 : 402-408.
34. Bharadwaj, K. G., Y. Hiyama, Y. Hu, L. A. Huggins, R. Ramakrishnan, N. A. Abumrad, G. I. Shulman, W. S. Blaner, and I. J. Goldberg. 2010. Chylomicron-And VLDL-derived lipids enter the heart through different pathways: in vivo evidence for receptor-And non-receptormediated fatty acid uptake. J. Biol. Chem. 285 : 37976-37986.
35. Wang, H., and R. H. Eckel. 2009. Lipoprotein lipase: from gene to obesity. Am. J. Physiol. Endocrinol. Metab. 297 : E271-E288.
36. Janssen, W. J., L. Barthel, A. Muldrow, R. E. Oberley-Deegan, M. T. Kearns, C. Jakubzick, and P. M. Henson. 2011. Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am. J. Respir. Crit. Care Med. 184 : 547-560.
37. Johnston, L. K., C. R. Rims, S. E. Gill, J. K. McGuire, and A. M. Manicone. 2012. Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am. J. Respir. Cell Mol. Biol. 47 : 417-426.
38. Schrage, A., C. Loddenkemper, U. Erben, U. Lauer, G. Hausdorf, P. R. Jungblut, J. Johnson, P. A. Knolle, M. Zeitz, A. Hamann, et al. 2008. Murine CD146 is widely expressed on endothelial cells and is recognized by the monoclonal antibody ME-9F1. Histochem. Cell Biol. 129 : 441-451.
39. Smadja, D. M., P. Gaussem, L. Mauge, D. Israel-Biet, F. Di gnat-George, S. Peyrard, G. Agnoletti, P. R. Vouhe, D. Bonnet, and M. Levy. 2009. Circulating endothelial cells: a new candidate biomarker of irreversible pulmonary hypertension secondary to congenital heart disease. Circulation. 119 : 374-381.
40. Bardin, N., V. Frances, V. Combes, J. Sampol, and F. Dignat-George. 1998. CD146: biosynthesis and production of a soluble form in human cultured endothelial cells. FEBS Lett. 421 : 12-14.
41. Boneberg, E. M., H. Illges, D. F. Legler, and G. Furstenberger. 2009. Soluble CD146 is generated by ectodomain shedding of membrane CD146 in a calcium-induced, matrix metalloprotease-dependent process. Microvasc. Res. 78 : 325-331.
42. Despoix, N., T. Walzer, N. Jouve, M. Blot-Chabaud, N. Bardin, P. Paul, L. Lyonnet, E. Vivier, F Dignat-George, and F. Vely. 2008. Mouse CD146/MCAM is a marker of natural killer cell maturation. Eur. J. Immunol. 38 : 2855-2864.
43. Sukonina, V., A. Lookene, T. Olivecrona, and G. Olivecrona. 2006. Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc. Natl. Acad. Sci. USA. 103 : 17450-17455.
44. Yoshida, K., T. Shimizugawa, M. Ono, and H. Furukawa. 2002. Angiopoietin-like protein 4 is a potent hyperlipidemia-inducing factor in mice and inhibitor of lipoprotein lipase. J. Lipid Res. 43 : 1770-1772.
45. Mandard, S., F. Zandbergen, E. van Straten, W. Wahli, F. Kuipers, M. Muller, and S. Kersten. 2006. The fasting-induced adipose factor/angiopoietin- like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J. Biol. Chem. 281 : 934-944.
46. Lichtenstein, L., and S. Kersten. 2010. Modulation of plasma TG lipolysis by Angiopoietin-like proteins and GPIHBP1. Biochim. Biophys. Acta. 1801 : 415-420.
47. Köster, A., Y. B. Chao, M. Mosior, A. Ford, P. A. Gonzalez-DeWhitt, J. E. Hale, D. Li, Y. Qiu, C. C. Fraser, D. D. Yang, et al. 2005. Transgenic angiopoietin-like (angptl)4 overexpression and targeted disruption of angptl4 and angptl3: regulation of triglyceride metabolism. Endocrinology. 146 : 4943-4950.
48. Shimizugawa, T., M. Ono, M. Shimamura, K. Yoshida, Y. Ando, R. Koishi, K. Ueda, T. Inaba, H. Minekura, T. Kohama, et al. 2002. ANGPTL3 decreases very low density lipoprotein triglyceride clearance by inhibition of lipoprotein lipase. J. Biol. Chem. 277 : 33742-33748.
49. Zhu, P., Y. Y. Goh, H. F. Chin, S. Kersten, and N. S. Tan. 2012. Angiopoietin-like 4: a decade of research. Biosci. Rep. 32 : 211-219.
50. Mattijssen, F., and S. Kersten. 2012. Regulation of triglyceride metabolism by Angiopoietin-like proteins. Biochim. Biophys. Acta. 1821 : 782-789.
51. Makoveichuk, E., V. Sukonina, O. Kroupa, P. Thulin, E. Ehrenborg, T. Olivecrona, and G. Olivecrona. 2012. Inactivation of lipoprotein lipase occurs on the surface of THP-1 macrophages where oligomers of angiopoietin-like protein 4 are formed. Biochem. Biophys. Res. Commun. 425 : 138-143.
52. Manalo, D. J., A. Rowan, T. Lavoie, L. Natarajan, B. D. Kelly, S. Q. Ye, J. G. Garcia, and G. L. Semenza. 2005. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 105 : 659-669.
53. Knowles, H. J., A. M. Cleton-Jansen, E. Korsching, and N. A. Athanasou. 2010. Hypoxia-inducible factor regulates osteoclastmediated bone resorption: role of angiopoietin-like 4. FASEB J. 24 : 4648-4659.
54. Wang, B., I. S. Wood, and P. Trayhurn. 2007. Dysregulation of the expression and secretion of infl ammation-related adipokines by hypoxia in human adipocytes. Pfl ugers Arch. 455 : 479-492.
55. Belanger, A. J., H. Lu, T. Date, L. X. Liu, K. A. Vincent, G. Y. Akita, S. H. Cheng, R. J. Gregory, and C. Jiang. 2002. Hypoxia up-regulates expression of peroxisome proliferator-Activated receptor gamma angiopoietin-related gene (PGAR) in cardiomyocytes: role of hypoxia inducible factor 1alpha. J. Mol. Cell. Cardiol. 34 : 765-774.
56. Li, H., C. Ge, F. Zhao, M. Yan, C. Hu, D. Jia, H. Tian, M. Zhu, T. Chen, G. Jiang, et al. 2011. Hypoxia-inducible factor 1 alpha-Activated angiopoietin-like protein 4 contributes to tumor metastasis via vascular cell adhesion molecule-1/integrin-1 signaling in human hepatocellular carcinoma. Hepatology. 54 : 910-919.
57. Zhang, H., C. C. Wong, H. Wei, D. M. Gilkes, P. Korangath, P. Chaturvedi, L. Schito, J. Chen, B. Krishnamachary, P. T. Winnard, Jr. ., et al. 2012. HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs. Oncogene. 31 : 1757-1770.
58. Drager, L.F., Q. Yao, K. L. Hernandez, M. K. Shin, S. Bevans-Fonti, J. Gay, T. E. Sussan, J. C. Jun, A. C. Myers, G. Olivecrona, et al. 2013. Chronic intermittent hypoxia induces atherosclerosis via activation of adipose Angiopoietin-like 4. Am. J. Respir. Crit. Care Med. Epub ahead of print. January 17, 2013; doi:10.1164/ rccm.201209-1688OC.
59. Lee, E. C., U. Desai, G. Gololobov, S. Hong, X. Feng, X. C. Yu, J. Gay, N. Wilganowski, C. Gao, L. L. Du, et al. 2009. Identifi cation of a new functional domain in angiopoietin-like 3 (ANGPTL3) and angiopoietin-like 4 (ANGPTL4) involved in binding and inhibition of lipoprotein lipase (LPL). J. Biol. Chem. 284 : 13735-13745.
60. Pohl, J., A. Ring, T. Hermann, and W. Stremmel. 2004. Role of FATP in parenchymal cell fatty acid uptake. Biochim. Biophys. Acta. 1686 : 1-6.
61. Fletcher, E. C., G. Bao, and C. C. Miller III. 1995. Effect of recurrent episodic hypocapnic, eucapnic, and hypercapnic hypoxia on systemic blood pressure. J. Appl. Physiol. 78 : 1516-1521.
62. Bao, G., N. Metreveli, R. Li, A. Taylor, and E. C. Fletcher. 1997. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J. Appl. Physiol. 83 : 95-101.
63. Kumar, G. K., V. Rai, S. D. Sharma, D. P. Ramakrishnan, Y. J. Peng, D. Souvannakitti, and N. R. Prabhakar. 2006. Chronic intermittent hypoxia induces hypoxia-evoked catecholamine effl ux in adult rat adrenal medulla via oxidative stress. J. Physiol. 575 : 229-239.
64. Dematteis, M., C. Julien, C. Guillermet, N. Sturm, S. Lantuejoul, M. Mallaret, P. Levy, and E. Gozal. 2008. Intermittent hypoxia induces early functional cardiovascular remodeling in mice. Am. J. Respir. Crit. Care Med. 177 : 227-235.
65. Julien, C., S. Bayat, and P. Levy. 2003. Vascular reactivity to norepinephrine and acetylcholine after chronic intermittent hypoxia in mice. Respir. Physiol. Neurobiol. 139 : 21-32.
66. Ranganathan, G., D. Phan, I. D. Pokrovskaya, J. E. McEwen, C. Li, and P. A. Kern. 2002. The translational regulation of lipoprotein lipase by epinephrine involves an RNA binding complex including the catalytic subunit of protein kinase A. J. Biol. Chem. 277 : 43281-43287.
67. Raynolds, M. V., P. D. Awald, D. F. Gordon, A. Gutierrez-Hartmann, D. C. Rule, W. M. Wood, and R. H. Eckel. 1990. Lipoprotein lipase gene expression in rat adipocytes is regulated by isoproterenol and insulin through different mechanisms. Mol. Endocrinol. 4 : 1416-1422.
68. Bartness, T. J., C. H. Vaughan, and C. K. Song. 2010. Sympathetic and sensory innervation of brown adipose tissue. Int. J. Obes. (Lond.). 34 (Suppl. 1) : S36-S42.
69. Mallampalli, R. K., R. G. Salome, S. L. Bowen, and D. A. Chappell. 1997. Very low density lipoproteins stimulate surfactant lipid synthesis in vitro. J. Clin. Invest. 99 : 2020-2029.
70. Rooney, S. A. 1985. The surfactant system and lung phospholipid biochemistry. Am. Rev. Respir. Dis. 131 : 439-460.
71. Sylvester, J. T., L. A. Shimoda, P. I. Aaronson, and J. P. Ward. 2012. Hypoxic pulmonary vasoconstriction. Physiol. Rev. 92 : 367-520.
72. Augustus, A. S., J. Buchanan, T. S. Park, K. Hirata, H. L. Noh, J. Sun, S. Homma, J. D'armiento, E. D. Abel, and I. J. Goldberg. 2006. Loss of lipoprotein lipase-derived fatty acids leads to increased cardiac glucose metabolism and heart dysfunction. J. Biol. Chem. 281 : 8716-8723.