Heparan sulfate deficiency disrupts developmental angiogenesis and causes congenital diaphragmatic hernia

Journal of Clinical Investigation

Volumn 124, Issue 1, 2014, Pages 209-221

  Zhang, Bing ^a   Xiao, Wenyuan ^a   Qiu, Hong ^a   Zhang, Fuming ^b   Moniz, Heather A ^a   Jaworski, Alexander ^c   Condac, Eduard ^a   Gutierrez Sanchez, Gerardo ^a   Heiss, Christian ^a   Clugston, Robin D ^d   Azadi, Parastoo ^a   Greer, John J ^d   Bergmann, Carl ^a   Moremen, Kelley W ^a   Li, Dean ^e   Linhardt, Robert J ^b   Esko, Jeffrey D ^f   Wang, Lianchun ^a  

^a University of Georgia   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c BROWN UNIVERSITY   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; HEPARAN SULFATE; MEMBRANE PROTEIN; N DEACETYLASE N SULFOTRANSFERASE 1; ROBO4 PROTEIN; SLIT PROTEIN; SLIT3 PROTEIN; SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONGENITAL DIAPHRAGM HERNIA; CONTROLLED STUDY; ENDOTHELIUM; FEMALE; GENE DISRUPTION; GENE DOSAGE; GENE INTERACTION; HETEROZYGOTE; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VASCULARIZATION;

EID: 84892914066     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71090     Document Type: Article

References (43)

1. Nobuhara KK, Lund DP, Mitchell J, Kharasch V, Wilson JM. Long-term outlook for survivors of congenital diaphragmatic hernia. Clin Perinatol. 1996;23(4):873-887.
2. Veenma DC, de Klein A, Tibboel D. Developmental and genetic aspects of congenital diaphragmatic hernia. Pediatr Pulmonol. 2012;47(6):534-545.
3. Brady PD, Srisupundit K, Devriendt K, Fryns JP, Deprest JA, Vermeesch Jr. Recent developments in the genetic factors underlying congenital diaphragmatic hernia. Fetal Diagn Ther. 2010;29(1):25-39.
4. Bielinska M, et al. Molecular genetics of congenital diaphragmatic defects. Ann Med. 2007; 39(4):261-274.
5. Clugston RD, Greer JJ. Diaphragm development and congenital diaphragmatic hernia. Semin Pediatr Surg. 2007;16(2):94-100.
6. Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. 2011;3(7):pii: a004952.
7. Pilia G, et al. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat Genet. 1996;12(3):241-247.
8. Wang L, Fuster M, Sriramarao P, Esko JD. Endothelial heparan sulfate deficiency impairs L-selectin- And chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol. 2005;6(9):902-910.
9. Fuster MM, et al. Genetic alteration of endothelial heparan sulfate selectively inhibits tumor angiogenesis. J Cell Biol. 2007;177(3):539-549.
10. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001;230(2):230-242.
11. Abramsson A, et al. Defective N-sulfation of heparan sulfate proteoglycans limits PDGF-BB binding and pericyte recruitment in vascular development. Genes Dev. 2007;21(3):316-331.
12. Stenzel D, Nye E, Nisancioglu M, Adams RH, Yamaguchi Y, Gerhardt H. Peripheral mural cell recruitment requires cell-Autonomous heparan sulfate. Blood. 2009;114(4):915-924.
13. Song JQ, Teng X, Cai Y, Tang CS, Qi YF. Activation of Akt/GSK-3beta signaling pathway is involved in intermedin(1-53) protection against myocardial apoptosis induced by ischemia/reperfusion. Apoptosis. 2009;14(11):1299-1307.
14. Fuster MM, Wang L. Endothelial heparan sulfate in angiogenesis. Prog Mol Biol Transl Sci. 2010; 93:179-212.
15. Shalaby F, et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376(6535):62-66.
16. Zhang B, Dietrich UM, Geng JG, Bicknell R, Esko JD, Wang L. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood. 2009; 114(19):4300-4309.
17. Park KW, et al. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev Biol. 2003; 261(1):251-267.
18. Jones CA, et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nature medicine. 2008;14(4):448-453.
19. Bedell VM, et al. roundabout4 is essential for angiogenesis in vivo. Proc Natl Acad Sci U S A. 2005; 102(18):6373-6378.
20. Huminiecki L, Gorn M, Suchting S, Poulsom R, Bicknell R. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics. 2002;79(4):547-552.
21. Klaassens M, et al. Congenital diaphragmatic hernia associated with duplication of 11q23-qter. Am J Med Genet A. 2006;140(14):1580-1586.
22. Wijelath E, et al. Multiple mechanisms for exogenous heparin modulation of vascular endothelial growth factor activity. J Cell Biochem. 2010; 111(2):461-468.
23. Zhang F, Ronca F, Linhardt RJ, Margolis RU. Structural determinants of heparan sulfate interactions with Slit proteins. Biochem Biophys Res Commun. 2004;317(2):352-357.
24. Liang Y, et al. Mammalian homologues of the Drosophila slit protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J Biol Chem. 1999; 274(25):17885-17892.
25. Fukuhara N, Howitt JA, Hussain SA, Hohenester E. Structural and functional analysis of slit and heparin binding to immunoglobulin-like domains 1 and 2 of Drosophila Robo. J Biol Chem. 2008; 283(23):16226-16234.
26. Hussain SA, et al. A molecular mechanism for the heparan sulfate dependence of slit-robo signaling. J Biol Chem. 2006;281(51):39693-39698.
27. Condac E, et al. The C-terminal fragment of axon guidance molecule Slit3 binds heparin and neutralizes heparin's anticoagulant activity. Glycobiology. 2012;22(9):1183-1192.
28. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 1991; 64(4):841-848.
29. DeBaun MR, Ess J, Saunders S. Simpson Golabi Behmel syndrome: progress toward understanding the molecular basis for overgrowth, malformation, and cancer predisposition. Mol Genet Metab. 2001; 72(4):279-286.
30. Eilken HM, Adams RH. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol. 2010;22(5):617-625.
31. Carmeliet P, et al. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat Med. 1999; 5(5):495-502.
32. Lavine KJ, et al. Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev. 2006;20(12):1651-1666.
33. Suchting S, Heal P, Tahtis K, Stewart LM, Bicknell R. Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration. FASEB J. 2005; 19(1):121-123.
34. Marlow R, et al. Vascular Robo4 restricts proangiogenic VEGF signaling in breast. Proc Natl Acad Sci U S A. 2010;107(23):10520-10525.
35. Koch AW, et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell. 2011;20(1):33-46.
36. Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature. 2005; 436(7048):193-200.
37. Yuan W, Rao Y, Babiuk RP, Greer JJ, Wu JY, Ornitz DM. A genetic model for a central (septum transversum) congenital diaphragmatic hernia in mice lacking Slit3. Proc Natl Acad Sci U S A. 2003; 100(9):5217-5222.
38. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999; 21(1):70-71.
39. Grunstein J, Masbad JJ, Hickey R, Giordano F, Johnson RS. Isoforms of vascular endothelial growth factor act in a coordinate fashion To recruit and expand tumor vasculature. Mol Cell Biol. 2000; 20(19):7282-7291.
40. Jaworski A, Burden SJ. Neuromuscular synapse formation in mice lacking motor neuron- And skeletal muscle-derived Neuregulin-1. J Neurosci. 2006; 26(2):655-661.
41. Zhang S, et al. Heparin-induced leukocytosis requires 6-O-sulfation and is caused by blockade of selectinand CXCL12 protein-mediated leukocyte trafficking in mice. J Biol Chem. 2012;287(8):5542-5553.
42. Wang L, Brown JR, Varki A, Esko JD. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- And P-selectins. J Clin Invest. 2002;110(1):127-136.
43. Zhang F, Moniz HA, Walcott B, Moremen KW, Linhardt RJ, Wang L. Characterization of the interaction between Robo1 and heparin and other glycosaminoglycans. Biochimie. 2013; pii:S0300-9084(13)00290-3.