Acute-phase protein α1-antitrypsin - A novel regulator of angiopoietin-like protein 4 transcription and secretion

Journal of Immunology

Volumn 192, Issue 11, 2014, Pages 5354-5362

  Frenzel, Eileen ^a   Wrenger, Sabine ^a   Immenschuh, Stephan ^a   Koczulla, Rembert ^b   Mahadeva, Ravi ^c   Deeg, H Joachim ^d,e   Dinarello, Charles A ^f   Welte, Tobias ^a   Q Marcondes, A Mario ^d,e   Janciauskiene, Sabina ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF WASHINGTON   (United States)

^e USA   (United States)

^f UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; ACUTE PHASE PROTEIN; ALPHA 1 ANTITRYPSIN; ALPHA 1 ANTITRYPSIN CONCENTRATE; ANGIOPOIETIN LIKE PROTEIN 4; GENISTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UO 126;

ADULT; ALPHA 1 ANTITRYPSIN DEFICIENCY; ARTICLE; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG EMPHYSEMA; MALE; MICROVASCULAR ENDOTHELIAL CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; UPREGULATION;

ALPHA 1-ANTITRYPSIN; ANGIOPOIETINS; ANILIDES; EMPHYSEMA; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LEUKOCYTES, MONONUCLEAR; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; SERINE PROTEINASE INHIBITORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84901273446     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400378     Document Type: Article

References (57)

1. 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.
2. Kim, I., H. G. Kim, H. Kim, H. H. Kim, S. K. Park, C. S. Uhm, Z. H. Lee, and G. Y. Koh. 2000. Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem. J. 346: 603-610.
3. Kersten, S., S. Mandard, N. S. Tan, P. Escher, D. Metzger, P. Chambon, F. J. Gonzalez, B. Desvergne, and W. Wahli. 2000. Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J. Biol. Chem. 275: 28488-28493.
4. Le Jan, S., C. Amy, A. Cazes, C. Monnot, N. Lamandé, J. Favier, J. Philippe, M. Sibony, J. M. Gasc, P. Corvol, and S. Germain. 2003. Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am. J. Pathol. 162: 1521-1528.
5. Lichtenstein, L., F. Mattijssen, N. J. de Wit, A. Georgiadi, G. J. Hooiveld, R. van der Meer, Y. He, L. Qi, A. Köster, J. T. Tamsma, et al. 2010. Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages. Cell Metab. 12: 580-592.
6. Lu, B., A. Moser, J. K. Shigenaga, C. Grunfeld, and K. R. Feingold. 2010. The acute phase response stimulates the expression of angiopoietin like protein 4. Biochem. Biophys. Res. Commun. 391: 1737-1741.
7. Grootaert, C., T. Van de Wiele, W. Verstraete, M. Bracke, and B. Vanhoecke. 2012. Angiopoietin-like protein 4: health effects, modulating agents and structure-function relationships. Expert Rev. Proteomics 9: 181-199.
8. Adachi, H., Y. Fujiwara, T. Kondo, T. Nishikawa, R. Ogawa, T. Matsumura, N. Ishii, R. Nagai, K. Miyata, M. Tabata, et al. 2009. Angptl 4 deficiency improves lipid metabolism, suppresses foam cell formation and protects against atherosclerosis. Biochem. Biophys. Res. Commun. 379: 806-811.
9. Hauton, D., and G. M. Caldwell. 2012. Cardiac lipoprotein lipase activity in the hypertrophied heart may be regulated by fatty acid flux. Biochim. Biophys. Acta 1821: 627-636.
10. Miida, T., and S. Hirayama. 2010. Impacts of angiopoietin-like proteins on lipoprotein metabolism and cardiovascular events. Curr. Opin. Lipidol. 21: 70-75.
11. Nettleton, J. A., K. A. Volcik, E.W. Demerath, E. Boerwinkle, and A. R. Folsom. 2008. Longitudinal changes in triglycerides according to ANGPTL4[E40K] genotype and longitudinal body weight change in the atherosclerosis risk in communities study. Ann. Epidemiol. 18: 842-846.
12. Talmud, P. J., M. Smart, E. Presswood, J. A. Cooper, V. Nicaud, F. Drenos, J. Palmen, M. G. Marmot, S. M. Boekholdt, N. J. Wareham, et al. 2008. ANGPTL4 E40K and T266M: effects on plasma triglyceride and HDL levels, postprandial responses, and CHD risk. Arterioscler. Thromb. Vasc. Biol. 28: 2319-2325.
13. Galaup, A., E. Gomez, R. Souktani, M. Durand, A. Cazes, C. Monnot, J. Teillon, S. Le Jan, C. Bouleti, G. Briois, et al. 2012. Protection against myocardial infarction and no-reflow through preservation of vascular integrity by angiopoietin-like 4. Circulation 125: 140-149.
14. Galaup, A., A. Cazes, S. Le Jan, J. Philippe, E. Connault, E. Le Coz, H. Mekid, L. M. Mir, P. Opolon, P. Corvol, et al. 2006. Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness. Proc. Natl. Acad. Sci. USA 103: 18721-18726.
15. 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 a-activated angiopoietin-like protein 4 contributes to tumor metastasis via vascular cell adhesion molecule-1/integrin b1 signaling in human hepatocellular carcinoma. Hepatology 54: 910-919.
16. Smart-Halajko, M. C., A. Kelley-Hedgepeth, M. C. Montefusco, J. A. Cooper, A. Kopin, J. M. McCaffrey, A. Balasubramanyam, H. J. Pownall, D. M. Nathan, I. Peter, et al. 2011. ANGPTL4 variants E40K and T266M are associated with lower fasting triglyceride levels in Non-Hispanic White Americans from the Look AHEAD Clinical Trial. BMC Med. Genet. 12: 89.
17. Xu, A., M. C. Lam, K. W. Chan, Y. Wang, J. Zhang, R. L. Hoo, J. Y. Xu, B. Chen, W. S. Chow, A.W. Tso, and K. S. Lam. 2005. Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc. Natl. Acad. Sci. USA 102: 6086-6091.
18. Goh, Y. Y., M. Pal, H. C. Chong, P. Zhu, M. J. Tan, L. Punugu, C. R. Lam, Y. H. Yau, C. K. Tan, R. L. Huang, et al. 2010. Angiopoietin-like 4 interacts with integrins beta1 and beta5 to modulate keratinocyte migration. Am. J. Pathol. 177: 2791-2803.
19. Goh, Y. Y., M. Pal, H. C. Chong, P. Zhu, M. J. Tan, L. Punugu, C. K. Tan, R. L. Huang, S. K. Sze, M. B. Tang, et al. 2010. Angiopoietin-like 4 interacts with matrix proteins to modulate wound healing. J. Biol. Chem. 285: 32999- 33009.
20. Stapleton, C. M., J. H. Joo, Y. S. Kim, G. Liao, R. A. Panettieri, Jr., and A. M. Jetten. 2010. Induction of ANGPTL4 expression in human airway smooth muscle cells by PMA through activation of PKC and MAPK pathways. Exp. Cell Res. 316: 507-516.
21. Wang, Y., H. Chen, H. Li, J. Zhang, and Y. Gao. 2013. Effect of angiopoietin-like protein 4 on rat pulmonary microvascular endothelial cells exposed to LPS. Int. J. Mol. Med. 32: 568-576.
22. 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 g angiopoietin-related gene (PGAR) in cardiomyocytes: role of hypoxia inducible factor 1a. J. Mol. Cell. Cardiol. 34: 765-774.
23. Kaddatz, K., T. Adhikary, F. Finkernagel, W. Meissner, S. Muller-Brusselbach, and R. Muller. 2010. Transcriptional profiling identifies functional interactions of TGF b and PPAR b/d signaling: synergistic induction of ANGPTL4 transcription. J. Biol. Chem. 285: 29469-29479.
24. Koliwad, S. K., T. Kuo, L. E. Shipp, N. E. Gray, F. Backhed, A. Y. So, R. V. Farese, Jr., and J. C. Wang. 2009. Angiopoietin-like 4 (ANGPTL4, fasting-induced adipose factor) is a direct glucocorticoid receptor target and participates in glucocorticoidregulated triglyceride metabolism. J. Biol. Chem. 284: 25593-25601.
25. Stockert, J., T. Adhikary, K. Kaddatz, F. Finkernagel, W. Meissner, S. Muller- russelbach, and R. Muller. 2011. Reverse crosstalk of TGFb and PPARb/d signaling identified by transcriptional profiling. Nucleic Acids Res. 39: 119-131.
26. Wiesner, G., R. E. Brown, G. S. Robertson, S. A. Imran, E. Ur, and M. Wilkinson. 2006. Increased expression of the adipokine genes resistin and fasting-induced adipose factor in hypoxic/ischaemic mouse brain. Neuroreport 17: 1195-1198.
27. Yoon, J. C., T. W. Chickering, E. D. Rosen, B. Dussault, Y. Qin, A. Soukas, J. M. Friedman, W. E. Holmes, and B. M. Spiegelman. 2000. Peroxisome proliferator-activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol. Cell. Biol. 20: 5343-5349.
28. Georgiadi, A., Y. Wang, R. Stienstra, N. Tjeerdema, A. Janssen, A. Stalenhoef, J. A. van der Vliet, A. de Roos, J. T. Tamsma, J. W. Smit, et al. 2013. Overexpression of angiopoietin-like protein 4 protects against atherosclerosis development. Arterioscler. Thromb. Vasc. Biol. 33: 1529-1537.
29. Aldonyte, R., T. E. Hutchinson, B. Jin, M. Brantly, E. Block, J. Patel, and J. Zhang. 2008. Endothelial a-1-antitrypsin attenuates cigarette smoke induced apoptosis in vitro. COPD 5: 153-162.
30. Aldonyte, R., L. Jansson, and S. Janciauskiene. 2004. Concentration-dependent effects of native and polymerised a1-antitrypsin on primary human monocytes, in vitro. BMC Cell Biol. 5: 11.
31. Huang, H., S. C. Campbell, T. Nelius, D. F. Bedford, D. Veliceasa, N. P. Bouck, and O. V. Volpert. 2004. a1-Antitrypsin inhibits angiogenesis and tumor growth. Int. J. Cancer 112: 1042-1048.
32. Janciauskiene, S., S. Wrenger, and T. Welte. 2012. Conformational and functional polymorphism of a1-antitrypsin: role in health and diseases. In Serine Proteases: Mechanism, Structure and Evolution. Isamu Chiba, and Takao Kamio, eds. Nova Publishers, Hauppauge, New York, p. 1-84
33. Van Molle, W., C. Libert, W. Fiers, and P. Brouckaert. 1997. Alpha 1-acid glycoprotein and a1-antitrypsin inhibit TNF-induced but not anti-Fas-induced apoptosis of hepatocytes in mice. J. Immunol. 159: 3555-3564.
34. Sabina, J., and W. Tobias. 2013. Augmentation therapy with a1-antitrypsin: novel perspectives. Cardiovasc. Hematol. Disord. Drug Targets 13: 90-98.
35. Talmud, P. J., S. Martin, G. Steiner, D. M. Flavell, D. B. Whitehouse, S. Nagl, R. Jackson, M. R. Taskinen, M. H. Frick, M. S. Nieminen, et al. 2003. Progression of atherosclerosis is associated with variation in the a1-antitrypsin gene. Arterioscler. Thromb. Vasc. Biol. 23: 644-649.
36. Kalis, M., R. Kumar, S. Janciauskiene, A. Salehi, and C. M. Cilio. 2010. a 1- Antitrypsin enhances insulin secretion and prevents cytokine-mediated apoptosis in pancreatic b-cells. Islets 2: 185-189.
37. Petrache, I., I. Fijalkowska, T. R. Medler, J. Skirball, P. Cruz, L. Zhen, H. I. Petrache, T. R. Flotte, and R.M. Tuder. 2006. alpha-1 antitrypsin inhibits caspase- 3 activity, preventing lung endothelial cell apoptosis. Am. J. Pathol. 169: 1155-1166.
38. Fregonese, L., and J. Stolk. 2008. Hereditary a-1-antitrypsin deficiency and its clinical consequences. Orphanet J. Rare Dis. 3: 16.
39. Lewis, E. C. 2012. Expanding the clinical indications for a(1)-antitrypsin therapy. Mol. Med. 18: 957-970.
40. Marcondes, A. M., X. Li, L. Tabellini, M. Bartenstein, J. Kabacka, G. E. Sale, J. A. Hansen, C. A. Dinarello, and H. J. Deeg. 2011. Inhibition of IL-32 activation by a-1 antitrypsin suppresses alloreactivity and increases survival in an allogeneic murine marrow transplantation model. Blood 118: 5031-5039.
41. Jonigk, D., M. Al-Omari, L. Maegel, M. Muller, N. Izykowski, J. Hong, K. Hong, S. H. Kim, M. Dorsch, R. Mahadeva, et al. 2013. Anti-inflammatory and immunomodulatory properties of a1-antitrypsin without inhibition of elastase. Proc. Natl. Acad. Sci. USA 110: 15007-15012.
42. Al-Omari, M., E. Korenbaum, M. Ballmaier, U. Lehmann, D. Jonigk, D. J. Manstein, T. Welte, R. Mahadeva, and S. Janciauskiene. 2011. Acute-phase protein a1-antitrypsin inhibits neutrophil calpain I and induces random migration. Mol. Med. 17: 865-874.
43. Zhang, Q. L., B. R. Cui, H. Y. Li, P. Li, L. Hong, L. P. Liu, D. Z. Ding, and X. Cui. 2013. MAPK and PI3K pathways regulate hypoxia-induced atrial natriuretic peptide secretion by controlling HIF-1a expression in beating rabbit atria. Biochem. Biophys. Res. Commun. 438: 507-512.
44. Subramaniyam, D., H. Zhou, M. Liang, T. Welte, R. Mahadeva, and S. Janciauskiene. 2010. Cholesterol rich lipid raft microdomains are gateway for acute phase protein, SERPINA1. Int. J. Biochem. Cell Biol. 42: 1562-1570.
45. Mandard, S., F. Zandbergen, N. S. Tan, P. Escher, D. Patsouris, W. Koenig, R. Kleemann, A. Bakker, F. Veenman, W. Wahli, et al. 2004. The direct peroxisome proliferator-activated receptor target fasting-induced adipose factor (FIAF/PGAR/ANGPTL4) is present in blood plasma as a truncated protein that is increased by fenofibrate treatment. J. Biol. Chem. 279: 34411-34420.
46. Takahashi, H., K. Fujita, T. Fujisawa, K. Yonemitsu, A. Tomimoto, I. Ikeda, M. Yoneda, T. Masuda, K. Schaefer, L. J. Saubermann, et al. 2006. Inhibition of peroxisome proliferator-activated receptor g activity in esophageal carcinoma cells results in a drastic decrease of invasive properties. Cancer Sci. 97: 854-860.
47. Staiger, H., C. Haas, J. Machann, R. Werner, M. Weisser, F. Schick, F. Machicao, N. Stefan, A. Fritsche, and H. U. Häring. 2009. Muscle-derived angiopoietin-like protein 4 is induced by fatty acids via peroxisome proliferator-activated receptor (PPAR)-delta and is of metabolic relevance in humans. Diabetes 58: 579-589.
48. Robciuc, M. R., E. Tahvanainen, M. Jauhiainen, and C. Ehnholm. 2010. Quantitation of serum angiopoietin-like proteins 3 and 4 in a Finnish population sample. J. Lipid Res. 51: 824-831.
49. Sukonina, V., A. Lookene, T. Olivecrona, and G. Olivecrona. 2006. Angiopoietinlike protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc. Natl. Acad. Sci. USA 103: 17450-17455.
50. Yau, M. H., Y. Wang, K. S. Lam, J. Zhang, D. Wu, and A. Xu. 2009. A highly conserved motif within the NH2-terminal coiled-coil domain of angiopoietin-like protein 4 confers its inhibitory effects on lipoprotein lipase by disrupting the enzyme dimerization. J. Biol. Chem. 284: 11942-11952.
51. Li, M., T. W. Lee, A. P. Yim, T. S. Mok, and G. G. Chen. 2006. Apoptosis induced by troglitazone is both peroxisome proliferator-activated receptor-gammaand ERK-dependent in human non-small lung cancer cells. J. Cell. Physiol. 209: 428-438.
52. Prusty, D., B. H. Park, K. E. Davis, and S. R. Farmer. 2002. Activation of MEK/ ERK signaling promotes adipogenesis by enhancing peroxisome proliferatoractivated receptor gamma (PPARg) and C/EBPa gene expression during the differentiation of 3T3-L1 preadipocytes. J. Biol. Chem. 277: 46226-46232.
53. Knowles, H. J., A. M. Cleton-Jansen, E. Korsching, and N. A. Athanasou. 2010. Hypoxia-inducible factor regulates osteoclast-mediated bone resorption: role of angiopoietin-like 4. FASEB J. 24: 4648-4659.
54. Wenger, R. H. 2000. Mammalian oxygen sensing, signalling and gene regulation. J. Exp. Biol. 203: 1253-1263.
55. Conrad, P. W., T. L. Freeman, D. Beitner-Johnson, and D. E. Millhorn. 1999. EPAS1 trans-activation during hypoxia requires p42/p44 MAPK. J. Biol. Chem. 274: 33709-33713.
56. Richard, D. E., E. Berra, E. Gothié, D. Roux, and J. Pouysségur. 1999. p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1a (HIF-1a) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274: 32631-32637.
57. Tuder, R. M., S. M. Janciauskiene, and I. Petrache. 2010. Lung disease associated with a1-antitrypsin deficiency. Proc. Am. Thorac. Soc. 7: 381-386.