Angiopoietin-like 4: A decade of research

Bioscience Reports

Volumn 32, Issue 3, 2012, Pages 211-219

  Zhu, Pengcheng ^a   Goh, Yan Yih ^a   Chin, Hwee Fang Alison ^a   Kersten, Sander ^b   Tan, Nguan Soon ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Angiopoietin; Homoeostasis; Lipoprotein lipase; Peroxisome proliferator activated receptor; Reactive oxygen species; Triacylglycerol

Indexed keywords

ANGIOPOIETIN; ANGIOPOIETIN LIKE 4 PROTEIN; LIPOPROTEIN LIPASE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANGIOPOIETIN LIKE 4 GENE; BLOOD VESSEL PERMEABILITY; CARCINOGENESIS; CELL DIFFERENTIATION; ENERGY BALANCE; FOOD INTAKE; GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GLUCOSE HOMEOSTASIS; HUMAN; INFLAMMATORY DISEASE; INTESTINE FLORA; KIDNEY DISEASE; LIPID METABOLISM; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN PROCESSING; RESEARCH PRIORITY; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WOUND HEALING;

ANGIOPOIETINS; ANIMALS; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; ENERGY METABOLISM; GENE EXPRESSION; HUMANS; INFLAMMATION; KIDNEY DISEASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; WOUND HEALING;

EID: 84859450817     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20110102     Document Type: Review

References (67)

1. Kim, I., Kim, H. G., Kim, H., Kim, H. H., Park, S. K., Uhm, C. S., Lee, Z. H. and Koh, G. Y. (2000) Hepatic expression, synthesis and secretion of a novel fibrinogen/angiopoietin-related protein that prevents endothelial-cell apoptosis. Biochem. J. 346, 603-610 (Pubitemid 30171019)
2. Kersten, S., Mandard, S., Tan, N. S., Escher, P., Metzger, D., Chambon, P., Gonzalez, F. J., Desvergne, B. and Wahli, W. (2000) Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J. Biol. Chem. 275, 28488-28493
3. Yoon, J. C., Chickering, T. W., Rosen, E. D., Dussault, B., Qin, Y., Soukas, A., Friedman, J. M., Holmes, W. E. and Spiegelman, B. M. (2000) Peroxisome proliferator-activated receptor gamma target gene encoding a novel angiopoietin-related protein associated with adipose differentiation. Mol. Cell. Biol. 20, 5343-5349 (Pubitemid 30431587)
4. Clement, L. C., Avila-Casado, C., Macé, C., Soria, E., Bakker, W. W., Kersten, S. and Chugh, S. S. (2011) Podocyte-secreted angiopoietin-like-4 mediates proteinuria in glucocorticoid-sensitive nephrotic syndrome. Nat. Med. 17, 117-122
5. Yin, W., Romeo, S., Chang, S., Grishin, N. V., Hobbs, H. H. and Cohen, J. C. (2009) Genetic variation in ANGPTL4 provides insights into protein processing and function. J. Biol. Chem. 284, 13213-13222
6. Ge, H., Yang, G., Huang, L., Motola, D. L., Pourbahrami, T. and Li, C. (2004) Oligomerization and regulated proteolytic processing of angiopoietin-like protein 4. J. Biol. Chem. 279, 2038-2045 (Pubitemid 38084475)
7. Yau, M. H., Wang, Y., Lam, K. S. L., Zhang, J., Wu, D. and Xu, A. (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
8. Yang, Y. H., Wang, Y., Lam, K. S. L., Yau, M. H., Cheng, K. K. Y., Zhang, J., Zhu, W., Wu, D. and Xu, A. (2008) Suppression of the Raf/MEK/ERK signaling cascade and inhibition of angiogenesis by the carboxyl terminus of angiopoietin-like protein 4. Arterioscler. Thromb. Vasc. Biol. 28, 835-840 (Pubitemid 351544096)
9. Lei, X., Shi, F., Basu, D., Huq, A., Routhier, S., Day, R. and Jin, W. (2011) Proteolytic processing of angiopoietin-like protein 4 by proprotein convertases modulates its inhibitory effects on lipoprotein lipase activity. J. Biol. Chem. 286, 15747-15756
10. Mandard, S., Zandbergen, F., Tan, N. S., Escher, P., Patsouris, D., Koenig, W., Kleemann, R., Bakker, A., Veenman, F., Wahli, W. 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 (Pubitemid 39318067)
11. Valenzuela, D. M., Griffiths, J. A., Rojas, J., Aldrich, T. H., Jones, P. F., Zhou, H., McClain, J., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. et al. (1999) Angiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc. Natl. Acad. Sci. U.S.A. 96, 1904-1909 (Pubitemid 29117840)
12. Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., Sato, T. N. and Yancopoulos, G. D. (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180 (Pubitemid 27010101)
13. Li, C. (2006) Genetics and regulation of angiopoietin-like proteins 3 and 4. Curr. Opin. Lipidol. 17, 152-156
14. Goh, Y. Y., Pal, M., Chong, H. C., Zhu, P., Tan, M. J., Punugu, L., Lam, C. R. I., Yau, Y. H., Tan, C. K., Huang, R. L. et al. (2010) Angiopoietin-like 4 interacts with integrins beta1 and beta5 to modulate keratinocyte migration. Am. J. Pathol. 177, 2791-2803
15. Goh, Y. Y., Pal, M., Chong, H. C., Zhu, P., Tan, M. J., Punugu, L., Tan, C. K., Huang, R. L., Sze, S. K., Tang, M. B.Y. et al. (2010) Angiopoietin-like 4 interacts with matrix proteins to modulate wound healing. J. Biol. Chem. 285, 32999-33009
16. Mandard, S., Zandbergen, F., van Straten, E., Wahli, W., Kuipers, F., Müller, M. and Kersten, S. (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
17. Kersten, S., Lichtenstein, L., Steenbergen, E., Mudde, K., Hendriks, H. F.J., Hesselink, M. K., Schrauwen, P. and Müller, M. (2009) Caloric restriction and exercise increase plasma ANGPTL4 levels in humans via elevated free fatty acids. Arterioscler. Thromb. Vasc. Biol. 29, 969-974
18. Robciuc, M. R., Tahvanainen, E., Jauhiainen, M. and Ehnholm, C. (2010) Quantitation of serum angiopoietin-like proteins 3 and 4 in a Finnish population sample. J. Lipid Res. 51, 824-831
19. Dutton, S. and Trayhurn, P. (2008) Regulation of angiopoietin-like protein 4/fasting-induced adipose factor (ANGPTL4/FIAF) expression in mouse white adipose tissue and 3T3-L1 adipocytes. Br. J. Nutr. 100, 18-26
20. Wiesner, G., Morash, B. A., Ur, E. and Wilkinson, M. (2004) Food restriction regulates adipose-specific cytokines in pituitary gland but not in hypothalamus. J. Endocrinol. 180, R1-R6 (Pubitemid 38443403)
21. Lichtenstein, L., Berbée, J. F. P., van Dijk, S. J., van Dijk, K. W., Bensadoun, A., Kema, I. P., Voshol, P. J., Müller, M., Rensen, P. C. N. and Kersten, S. (2007) ANGPTL4 upregulates cholesterol synthesis in liver via inhibition of LPL- and HL-dependent hepatic cholesterol uptake. Arterioscler. Thromb. Vasc. Biol. 27, 2420-2427 (Pubitemid 350203959)
22. Koliwad, S. K., Kuo, T., Shipp, L. E., Gray, N. E., Backhed, F., So, A. Y. L., Farese, R. V. and Wang, J. C. (2009) Angiopoietin-like 4 (ANGPTL4, fasting-induced adipose factor) is a direct glucocorticoid receptor target and participates in glucocorticoid-regulated triglyceride metabolism. J. Biol. Chem. 284, 25593-25601
23. Stockert, J., Adhikary, T., Kaddatz, K., Finkernagel, F., Meissner, W., Müller-Brüsselbach, S. and Müller, R. (2011) Reverse crosstalk of TGFβ and PPARβ/δ signaling identified by transcriptional profiling. Nucleic Acids Res. 39, 119-131
24. Kaddatz, K., Adhikary, T., Finkernagel, F., Meissner, W., Müller-Brüsselbach, S. and Müller, R. (2010) Transcriptional profiling identifies functional interactions of TGFβ and PPARβ/δsignaling: synergistic induction of ANGPTL4 transcription. J. Biol. Chem. 285, 29469-29479
25. Peng, J. H. F., Feng, Y. and Rhodes, P. G. (2006) Down-regulation of phospholipase D2 mRNA in neonatal rat brainstem and cerebellum after hypoxia-ischemia. Neurochem. Res. 31, 1191-1196 (Pubitemid 44701765)
26. Wiesner, G., Brown, R. E., Robertson, G. S., Imran, S. A., Ur, E. and Wilkinson, M. (2006) Increased expression of the adipokine genes resistin and fasting-induced adipose factor in hypoxic/ischaemic mouse brain. NeuroReport 17, 1195-1198 (Pubitemid 44051412)
27. Wang, B., Wood, I. S. and Trayhurn, P. (2007) Dysregulation of the expression and secretion of inflammation-related adipokines by hypoxia in human adipocytes. Pflugers Arch. 455, 479-492 (Pubitemid 47624196)
28. Le, J., Amy, C., Cazes, A., Monnot, C., Lamande, N., Favier, J., Philippe, J., Sibony, M., Gasc, J., Corvol, P. and Germain, S. (2003) Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am. J. Pathol. 162, 1521-1528 (Pubitemid 36512834)
29. González-Muniesa, P., de Oliveira, C., Pérez de Heredia, F., Thompson, M. P. and Trayhurn, P. (2011) Fatty acids and hypoxia stimulate the expression and secretion of the adipokine ANGPTL4 (angiopoietin-like protein 4/ fasting-induced adipose factor) by human adipocytes. J. Nutrigenetics Nutrigenomics 4, 146-153
30. Murata, M., Yudo, K., Nakamura, H., Chiba, J., Okamoto, K., Suematsu, N., Nishioka, K., Beppu, M., Inoue, K., Kato, T. and Masuko, K. (2009) Hypoxia upregulates the expression of angiopoietin-like-4 in human articular chondrocytes: role of angiopoietin-like-4 in the expression of matrix metalloproteinases and cartilage degradation. J. Orthop. Res. 27, 50-57
31. Yoshida, K., Ono, M., Koishi, R. and Furukawa, H. (2004) Characterization of the 5′ regulatory region of the mouse angiopoietin-like protein 4. Vet. Res. Commun. 28, 299-305 (Pubitemid 39137430)
32. Xu, A., Lam, M. C., Chan, K. W., Wang, Y., Zhang, J., Hoo, R. L. C., Xu, J. Y., Chen, B., Chow, W. S., Tso, A. W. K. and Lam, K. S. L. (2005) Angiopoietin-like protein 4 decreases blood glucose and improves glucose tolerance but induces hyperlipidemia and hepatic steatosis in mice. Proc. Natl. Acad. Sci. U.S.A. 102, 6086-6091 (Pubitemid 40594259)
33. Padua, D., Zhang, X. H. F., Wang, Q., Nadal, C., Gerald, W. L., Gomis, R. R. and Massagué, J. (2008) TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133, 66-77 (Pubitemid 351442989)
34. Kim, H. K., Youn, B. S., Shin, M. S., Namkoong, C., Park, K. H., Baik, J. H., Kim, J. B., Park, J. Y., Lee, K. U., Kim, Y. B. and Kim, M. S. (2010) Hypothalamic ANGPTL4/FIAF is a novel regulator of food intake and body weight. Diabetes 59, 2772-2780
35. Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F. and Gordon, J. I. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U.S.A. 101, 15718-15723 (Pubitemid 39473554)
36. Fleissner, C. K., Huebel, N., Abd El-Bary, M. M., Loh, G., Klaus, S. and Blaut, M. (2010) Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br. J. Nutr. 104, 919-929
37. Aronsson, L., Huang, Y., Parini, P., Korach-André, M., Håkansson, J., Gustafsson, J. Å., Pettersson, S., Arulampalam, V. and Rafter, J. (2010) Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS ONE 5, e13087
38. Sonnenburg, W. K., Yu, D., Lee, E. C., Xiong, W., Gololobov, G., Key, B., Gay, J., Wilganowski, N., Hu, Y., Zhao, S., Schneider, M. et al. (2009) GPIHBP1 stabilizes lipoprotein lipase and prevents its inhibition by angiopoietin-like 3 and angiopoietin-like 4. J. Lipid Res. 50, 2421-2429
39. Georgiadi, A., Lichtenstein, L., Degenhardt, T., Boekschoten, M. V., van Bilsen, M., Desvergne, B., Müller, M. and Kersten, S. (2010) Induction of cardiac ANGPTL4 by dietary fatty acids is mediated by peroxisome proliferator-activated receptor beta/delta and protects against fatty acid-induced oxidative stress. Circ. Res. 106, 1712-1721
40. Staiger, H., Haas, C., Machann, J., Werner, R., Weisser, M., Schick, F., Machicao, F., Stefan, N., Fritsche, A. and Häring, H. U. (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
41. Sanderson, L. M., Degenhardt, T., Koppen, A., Kalkhoven, E., Desvergne, B., Müller, M. and Kersten, S. (2009) Peroxisome proliferator-activated receptor beta/delta (PPARbeta/delta) but not PPARalpha serves as a plasma free fatty acid sensor in liver. Mol. Cell. Biol. 29, 6257-6267
42. Robciuc, M. R., Naukkarinen, J., Ortega-Alonso, A., Tyynismaa, H., Raivio, T., Rissanen, A., Kaprio, J., Ehnholm, C., Jauhiainen, M. and Pietiläinen, K. H. (2011) Serum angiopoietin-like 4 protein levels and expression in adipose tissue are inversely correlated with obesity in monozygotic twins. J. Lipid Res. 52, 1575-1582
43. Koster, A., Chao, Y., Mosior, M., Ford, A., Gonzalez-DeWhitt, P., Hale, J., Li, D., Qiu, Y., Fraser, C. and Yang, D. (2005) Transgenic angiopoietin-like (ANGPTL)4 overexpression and targeted disruption of ANGPTL4 and ANGPTL regulation of triglyceride metabolism. Endocrinology 146, 4943-4950 (Pubitemid 41446633)
44. Smart-Halajko, M. C., Robciuc, M. R., Cooper, J. A., Jauhiainen, M., Kumari, M., Kivimaki, M., Khaw, K. T., Boekholdt, S. M., Wareham, N. J., Gaunt, T. R. et al. (2010) The relationship between plasma angiopoietin-like protein 4 levels, angiopoietin-like protein 4 genotype, and coronary heart disease risk. Arterioscler. Thromb. Vasc. Biol. 30, 2277-2282
45. Talmud, P. J., Smart, M., Presswood, E., Cooper, J. A., Nicaud, V., Drenos, F., Palmen, J., Marmot, M. G., Boekholdt, S. M., Wareham, N. J. 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
46. Romeo, S., Pennacchio, L. A., Fu, Y., Boerwinkle, E., Tybjaerg-Hansen, A., Hobbs, H. H. and Cohen, J. C. (2007) Population-based resequencing of ANGPTL4 uncovers variations that reduce triglycerides and increase HDL. Nat. Genet. 39, 513-516 (Pubitemid 46514768)
47. Kathiresan, S., Willer, C. J., Peloso, G. M., Demissie, S., Musunuru, K., Schadt, E. E., Kaplan, L., Bennett, D., Li, Y., Tanaka, T. et al. (2009) Common variants at 30 loci contribute to polygenic dyslipidemia. Nat. Genet. 41, 56-65
48. Lichtenstein, L., Mattijssen, F., de Wit, N. J., Georgiadi, A., Hooiveld, G. J., van der Meer, R., He, Y., Qi, L., Köster, A., Tamsma, J. T. 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
49. Lu, B., Moser, A., Shigenaga, J. K., Grunfeld, C. and Feingold, K. R. (2010) The acute phase response stimulates the expression of angiopoietin like protein 4. Biochem. Biophys. Res. Commun. 391, 1737-1741
50. Reiser, J. (2011) Filtering new facts about kidney disease. Nat. Med. 17, 44-45
51. Werner, S. and Grose, R. (2003) Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83, 835-870 (Pubitemid 36828927)
52. Pal, M., Tan, M., Huang, R., Goh, Y., Wang, X., Tang, M. and Tan, N. (2011) Angiopoietin-like 4 regulates epidermal differentiation. PLoS ONE 6, e25377
53. Hu, Z., Fan, C., Livasy, C., He, X., Oh, D. S., Ewend, M. G., Carey, L. A., Subramanian, S., West, R., Ikpatt, F. et al. (2009) A compact VEGF signature associated with distant metastases and poor outcomes. BMC Med. 7, 9
54. Nakayama, T., Hirakawa, H., Shibata, K., Nazneen, A., Abe, K., Nagayasu, T. and Taguchi, T. (2011) Expression of angiopoietin-like 4 (ANGPTL4) in human colorectal cancer: ANGPTL4 promotes venous invasion and distant metastasis. Oncol. Rep. 25, 929-935
55. Le Jan, S., Amy, C., Cazes, A., Monnot, C., Lamandé, N., Favier, J., Philippe, J., Sibony, M., Gasc, J. M., Corvol, P. and Germain, S. (2003) Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am. J. Pathol. 162, 1521-1528 (Pubitemid 36512834)
56. 2 ratio and confers anoikis resistance to tumors. Cancer Cell 19, 401-415
57. Shibata, K., Nakayama, T., Hirakawa, H., Hidaka, S. and Nagayasu, T. (2010) Clinicopathological significance of angiopoietin-like protein 4 expression in oesophageal squamous cell carcinoma. J. Clin. Pathol. 63, 1054-1058
58. Desai, U., Lee, E. C., Chung, K., Gao, C., Gay, J., Key, B., Hansen, G., Machajewski, D., Platt, K. A., Sands, A. T. et al. (2007) Lipid-lowering effects of anti-angiopoietin-like 4 antibody recapitulate the lipid phenotype found in angiopoietinlike 4 knockout mice. Proc. Natl. Acad. Sci. U.S.A. 104, 11766-11771 (Pubitemid 47175087)
59. Zhang, Z., Cao, L., Li, J., Liang, X., Liu, Y., Liu, H., Du, J., Qu, Z., Cui, M., Liu, S. et al. (2008) Acquisition of anoikis resistance reveals a synoikis-like survival style in BEL7402 hepatoma cells. Cancer Lett. 267, 106-115
60. Gealekman, O., Burkart, A., Chouinard, M., Nicoloro, S. M., Straubhaar, J. and Corvera, S. (2008) Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production. Am. J. Physiol. Endocrinol. Metab. 295, E1056-E1064
61. Marmé, D. (2001) Tumor angiogenesis: new approaches to cancer therapy. Onkologie 24 (Suppl. 1), 1-5
62. Gomez Perdiguero, E., Galaup, A., Durand, M., Teillon, J., Philippe, J., Valenzuela, D. M., Murphy, A. J., Yancopoulos, G. D., Thurston, G. and Germain, S. (2011) Alteration of developmental and pathological retinal angiogenesis in ANGPTL4-deficient mice. J. Biol. Chem. 286, 36841-36851
63. Ito, Y., Oike, Y., Yasunaga, K., Hamada, K., Miyata, K., Matsumoto, S. I., Sugano, S., Tanihara, H., Masuho, Y. and Suda, T. (2003) Inhibition of angiogenesis and vascular leakiness by angiopoietin-related protein 4. Cancer Res. 63, 6651-6657 (Pubitemid 37322943)
64. Cazes, A., Galaup, A., Chomel, C., Bignon, M., Bréchot, N., Le Jan, S., Weber, H., Corvol, P., Muller, L., Germain, S. and Monnot, C. (2006) Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton. Circ. Res. 99, 1207-1215 (Pubitemid 44808657)
65. Galaup, A., Cazes, A., Le Jan, S., Philippe, J., Connault, E., Le Coz, E., Mekid, H., Mir, L. M., Opolon, P., Corvol, P. et al. (2006) Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness. Proc. Natl. Acad. Sci. U.S.A. 103, 18721-18726 (Pubitemid 44913477)
66. Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L. and Massagué, J. (2005) Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524 (Pubitemid 41112921)
67. Huang, R. L., Teo, Z., Chong, H. C., Zhu, P., Tan, M. J., Tan, C. K., Lam, C. R. I., Sng, M. K., Leong, D. T. W., Tan, S. M. et al. (2011) ANGPTL4 modulates vascular junction integrity by integrin signaling and disruption of intercellular VE-cadherin and claudin-5 clusters. Blood 118, 3990-4002