ApoB-containing lipoproteins regulate angiogenesis by modulating expression of VEGF receptor 1

Nature Medicine

Volumn 18, Issue 6, 2012, Pages 967-973

  Avraham Davidi, Inbal ^a   Ely, Yona ^a   Pham, Van N ^b   Castranova, Daniel ^b   Grunspan, Moshe ^a   Malkinson, Guy ^a   Gibbs Bar, Liron ^a   Mayseless, Oded ^a   Allmog, Gabriella ^a   Lo, Brigid ^b   Warren, Carmen M ^c   Chen, Tom T ^c   Ungos, Josette ^b   Kidd, Kameha ^b   Shaw, Kenna ^b   Rogachev, Ilana ^a   Wan, Wuzhou ^d   Murphy, Philip M ^d   Farber, Steven A ^e   Carmel, Liran ^f   Shelness, Gregory S ^g   Iruela Arispe, M Luisa ^c   Weinstein, Brant M ^b   Yaniv, Karina ^a   more..

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e GEOPHYSICAL LABORATORY   (United States)

^f HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^g WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE; HUMAN; HUMAN CELL; HYPERLIPIDEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; APOLIPOPROTEIN C-II; APOLIPOPROTEINS B; BACTERIAL PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; HUMANS; LIPOPROTEINS; LIPOPROTEINS, LDL; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; ZEBRAFISH;

DANIO RERIO; MUS;

EID: 84862005373     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2759     Document Type: Article

References (53)

1. Yaniv, K. et al. Live imaging of lymphatic development in the zebrafish. Nat. Med. 12, 711-716 (2006). (Pubitemid 43865243)
2. Lawson, N.D. & Weinstein, B.M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318 (2002). (Pubitemid 35002091)
3. Hussain, M.M. et al. Microsomal triglyceride transfer protein in plasma and cellular lipid metabolism. Curr. Opin. Lipidol. 19, 277-284 (2008). (Pubitemid 351653566)
4. Raabe, M. et al. Knockout of the abetalipoproteinemia gene in mice: reduced lipoprotein secretion in heterozygotes and embryonic lethality in homozygotes. Proc. Natl. Acad. Sci. USA 95, 8686-8691 (1998). (Pubitemid 28350549)
5. Marza, E. et al. Developmental expression and nutritional regulation of a zebrafish gene homologous to mammalian microsomal triglyceride transfer protein large subunit. Dev. Dyn. 232, 506-518 (2005). (Pubitemid 40129804)
6. Schlegel, A. & Stainier, D.Y. Microsomal triglyceride transfer protein is required for yolk lipid utilization and absorption of dietary lipids in zebrafish larvae. Biochemistry 45, 15179-15187 (2006). (Pubitemid 46032444)
7. Stoletov, K. et al. Vascular lipid accumulation, lipoprotein oxidation, and macrophage lipid uptake in hypercholesterolemic zebrafish. Circ. Res. 104, 952-960 (2009).
8. Schlegel, A. & Stainier, D.Y. Lessons from "lower" organisms: what worms, flies, and zebrafish can teach us about human energy metabolism. PLoS Genet. 3, e199 (2007).
9. Shelton, J.M., Lee, M.H., Richardson, J.A. & Patel, S.B. Microsomal triglyceride transfer protein expression during mouse development. J. Lipid Res. 41, 532-537 (2000). (Pubitemid 30220656)
10. Babin, P.J. & Gibbons, G.F. The evolution of plasma cholesterol: direct utility or a "spandrel" of hepatic lipid metabolism? Prog. Lipid Res. 48, 73-91 (2009).
11. Babin, P.J. et al. Both apolipoprotein E and A-I genes are present in a nonmammalian vertebrate and are highly expressed during embryonic development. Proc. Natl. Acad. Sci. USA 94, 8622-8627 (1997). (Pubitemid 27335089)
12. Thorpe, J.L., Doitsidou, M., Ho, S.Y., Raz, E. & Farber, S.A. Germ cell migration in zebrafish is dependent on HMGCoA reductase activity and prenylation. Dev. Cell 6, 295-302 (2004). (Pubitemid 38190367)
13. Amack, J.D. & Yost, H.J. The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr. Biol. 14, 685-690 (2004). (Pubitemid 38503605)
14. Berriot-Varoqueaux, N., Aggerbeck, L.P., Samson-Bouma, M. & Wetterau, J.R. The role of the microsomal triglygeride transfer protein in abetalipoproteinemia. Annu. Rev. Nutr. 20, 663-697 (2000).
15. Shoulders, C.C. et al. Abetalipoproteinemia is caused by defects of the gene encoding the 97 kDa subunit of a microsomal triglyceride transfer protein. Hum. Mol. Genet. 2, 2109-2116 (1993). (Pubitemid 24003406)
16. Rader, D.J. & Brewer, H.B. Jr. Abetalipoproteinemia. New insights into lipoprotein assembly and vitamin E metabolism from a rare genetic disease. J. Am. Med. Assoc. 270, 865-869 (1993). (Pubitemid 23234117)
17. Farber, S.A. et al. Genetic analysis of digestive physiology using fluorescent phospholipid reporters. Science 292, 1385-1388 (2001). (Pubitemid 32476227)
18. Pickart, M.A. et al. Genome-wide reverse genetics framework to identify novel functions of the vertebrate secretome. PLoS ONE 1, e104 (2006).
19. Anderson, J.L., Carten, J.D. & Farber, S.A. Zebrafish lipid metabolism: from mediating early patterning to the metabolism of dietary fat and cholesterol. Methods Cell Biol. 101, 111-141 (2011).
20. Breckenridge, W.C. Apolipoprotein C-II deficiency. Adv. Exp. Med. Biol. 201, 211-226 (1986).
21. Hegele, R.A. et al. An apolipoprotein CII mutation, CIILys19-Thr' identified in patients with hyperlipidemia. Dis. Markers 9, 73-80 (1991).
22. Sethuraman, G. et al. Familial homozygous hypercholesterolemia: report of two patients and review of the literature. Pediatr. Dermatol. 24, 230-234 (2007). (Pubitemid 46848941)
23. Hegele, R.A. Plasma lipoproteins: genetic influences and clinical implications. Nat. Rev. Genet. 10, 109-121 (2009).
24. Connelly, P.W., Maguire, G.F. & Little, J.A. Apolipoprotein CIISt. Michael. Familial apolipoprotein CII deficiency associated with premature vascular disease. J. Clin. Invest. 80, 1597-1606 (1987). (Pubitemid 18007130)
25. Landmesser, U., Hornig, B. & Drexler, H. Endothelial dysfunction in hypercholesterolemia: mechanisms, pathophysiological importance, and therapeutic interventions. Semin. Thromb. Hemost. 26, 529-537 (2000).
26. Henry, P.D. Hypercholesterolemia and angiogenesis. Am. J. Cardiol. 72, 61C-64C (1993). (Pubitemid 23272008)
27. Fazio, S. & Linton, M.F. Mouse models of hyperlipidemia and atherosclerosis. Front. Biosci. 6, D515-D525 (2001).
28. Wouters, K., Shiri-Sverdlov, R., van Gorp, P.J., van Bilsen, M. & Hofker, M.H. Understanding hyperlipidemia and atherosclerosis: lessons from genetically modified Apoe and Ldlr mice. Clin. Chem. Lab. Med. 43, 470-479 (2005). (Pubitemid 41460623)
29. Hiratsuka, S., Minowa, O., Kuno, J., Noda, T. & Shibuya, M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. USA 95, 9349-9354 (1998). (Pubitemid 28506234)
30. Kearney, J.B. et al. Vascular endothelial growth factor receptor Flt-1 negatively regulates developmental blood vessel formation by modulating endothelial cell division. Blood 99, 2397-2407 (2002). (Pubitemid 34525425)
31. Chappell, J.C., Taylor, S.M., Ferrara, N. & Bautch, V.L. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev. Cell 17, 377-386 (2009).
32. Bussman, J. et al. Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 137, 2653-2657 (2010).
33. Shelness, G.S., Hou, L., Ledford, A.S., Parks, J.S. & Weinberg, R.B. Identification of the lipoprotein initiating domain of apolipoprotein B. J. Biol. Chem. 278, 44702-44707 (2003). (Pubitemid 37377227)
34. Hessler, J.R., Robertson, A.L. Jr. & Chisolm, G.M. III. LDL-induced cytotoxicity and its inhibition by HDL in human vascular smooth muscle and endothelial cells in culture. Atherosclerosis 32, 213-229 (1979). (Pubitemid 9129780)
35. Usui, R., Shibuya, M., Ishibashi, S. & Maru, Y. Ligand-independent activation of vascular endothelial growth factor receptor 1 by low-density lipoprotein. EMBO Rep. 8, 1155-1161 (2007). (Pubitemid 350201734)
36. Ylä-Herttuala, S. & Alitalo, K. On the relationship of LDL and VEGFR1: not just a family affair. EMBO Rep. 8, 1127-1128 (2007). (Pubitemid 350201729)
37. Arany, Z. et al. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature 451, 1008-1012 (2008). (Pubitemid 351301733)
38. Fraisl, P., Baes, M. & Carmeliet, P. Hungry for blood vessels: linking metabolism and angiogenesis. Dev. Cell 14, 313-314 (2008).
39. Hagberg, C.E. et al. Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature 464, 917-921 (2010).
40. Isogai, S., Lawson, N.D., Torrealday, S., Horiguchi, M. & Weinstein, B.M. Angiogenic network formation in the developing vertebrate trunk. Development 130, 5281-5290 (2003). (Pubitemid 37369685)
41. Roman, B.L. et al. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129, 3009-3019 (2002). (Pubitemid 34874278)
42. Isogai, S., Horiguchi, M. & Weinstein, B.M. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230, 278-301 (2001). (Pubitemid 32171423)
43. Shireman, R., Kilgore, L.L. & Fisher, W.R. Solubilization of apolipoprotein B and its specific binding by the cellular receptor for low density lipoprotein. Proc. Natl. Acad. Sci. USA 74, 5150-5154 (1977). (Pubitemid 8239064)
44. Nicoli, S., De Sena, G. & Presta, M. Fibroblast growth factor 2-induced angiogenesis in zebrafish: the zebrafish yolk membrane (ZFYM) angiogenesis assay. J. Cell. Mol. Med. 13, 2061-2068 (2009).
45. Habeck, H., Odenthal, J., Walderich, B., Maischein, H. & Schulte-Merker, S. Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr. Biol. 12, 1405-1412 (2002). (Pubitemid 34915543)
46. Bligh, E.G. & Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917 (1959).
47. Itkin, M. et al. GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23, 4507-4525 (2011).
48. Pham, V.N. et al. Combinatorial function of ETS transcription factors in the developing vasculature. Dev. Biol. 303, 772-783 (2007). (Pubitemid 46341274)
49. Takada, N. & Appel, B. Identification of genes expressed by zebrafish oligodendrocytes using a differential microarray screen. Dev. Dyn. 239, 2041-2047 (2010).
50. Zygmunt, T. et al. Semaphorin-PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev. Cell 21, 301-314 (2011).
51. Hansen, M.B., Nielsen, S.E. & Berg, K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 119, 203-210 (1989). (Pubitemid 19132276)
52. Sellers, J.A., Hou, L., Athar, H., Hussain, M.M. & Shelness, G.S. A Drosophila microsomal triglyceride transfer protein homolog promotes the assembly and secretion of human apolipoprotein B. Implications for human and insect transport and metabolism. J. Biol. Chem. 278, 20367-20373 (2003). (Pubitemid 36799237)
53. Gore, A.V., Lampugnani, M.G., Dye, L., Dejana, E. & Weinstein, B.M. Combinatorial interaction between CCM pathway genes precipitates hemorrhagic stroke. Dis. Model Mech. 1, 275-281 (2008).