Peripheral mural cell recruitment requires cell-autonomous heparan sulfate

Blood

Volumn 114, Issue 4, 2009, Pages 915-924

  Stenzel, Denise ^a   Nye, Emma ^a   Nisancioglu, Maya ^b   Adams, Ralf H ^c   Yamaguchi, Yu ^d   Gerhardt, Holger ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARAN SULFATE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; EXOSTOSIN 1; EXOSTOSIN-1; N ACETYLGLUCOSAMINYLTRANSFERASE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLEEDING; CELL LOSS; CELL MIGRATION; CELL POLARITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EDEMA; GENETIC ANALYSIS; MORPHOLOGY; MOUSE; MURAL CELL; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SMOOTH MUSCLE; STEM CELL; SYNTHESIS; VASCULAR DISEASE; ANIMAL; ANIMAL EMBRYO; AUTOCRINE EFFECT; BLOOD VESSEL; C57BL MOUSE; CELL ADHESION; CELL MOTION; CONGENITAL MALFORMATION; DRUG EFFECT; ENDOTHELIUM CELL; GENE DELETION; GENETICS; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALS; AUTOCRINE COMMUNICATION; BLOOD VESSELS; CELL ADHESION; CELL MOVEMENT; CENTRAL NERVOUS SYSTEM; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; GENE DELETION; HEPARITIN SULFATE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA;

EID: 68249161282     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-10-186239     Document Type: Article

References (41)

1. Abramsson A, Kurup S, Busse M, et al. Defective N-sulfation of heparan sulfate proteoglycans limits PDGF-BB binding and pericyte recruitment in vascular development. Genes Dev. 2007;21:316-331. (Pubitemid 46246780)
2. Hammes HP. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res. 2005;37[suppl 1]:39-43.
3. von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res. 2006;312:623-629.
4. Hirschi KK, Burt JM, Hirschi KD, Dai C. Gap junction communication mediates transforming growth factor-beta activation and endothelial-induced mural cell differentiation. Circ Res. 2003;93:429-437. (Pubitemid 37100008)
5. Yang X, Castilla LH, Xu X, et al. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development. 1999;126:1571-1580. (Pubitemid 29204322)
6. Rudini N, Felici A, Giampietro C, et al. VE-cadherin is a critical endothelial regulator of TGF-beta signalling. EMBO J. 2008;27:993-1004.
7. Cavallaro U, Liebner S, Dejana E. Endothelial cadherins and tumor angiogenesis. Exp Cell Res. 2006;312:659-667.
8. Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277:242-245. (Pubitemid 27446080)
9. Hellström M, Gerhardt H, Kalén M, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol. 2001;153:543-553. (Pubitemid 34280141)
10. Abramsson A, Lindblom P, Betsholtz C. Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest. 2003;112:1142-1151. (Pubitemid 38056291)
11. Lindblom P, Gerhardt H, Liebner S, et al. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev. 2003;17:1835-1840. (Pubitemid 36944561)
12. Kurup S, Abramsson A, Li JP, et al. Heparan sulphate requirement in platelet-derived growth factor B-mediated pericyte recruitment. Biochem Soc Trans. 2006;34:454-455. (Pubitemid 43954010)
13. Foo SS, Turner CJ, Adams S, et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel- wall assembly. Cell. 2006;124:161-173. (Pubitemid 43069317)
14. Inatani M, Irie F, Plump AS, Tessier-Lavigne M, Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science. 2003;302:1044-1046. (Pubitemid 37386197)
15. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999;21:70-71. (Pubitemid 29036285)
16. Gerhardt H, Golding M, Fruttiger M, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161:1163-1177. (Pubitemid 36870177)
17. Ruhrberg C, Gerhardt H, Golding M, et al. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 2002;16:2684-2698.
18. Abraham S, Kogata N, Fassler R, Adams RH. Integrin beta1 subunit controls mural cell adhesion, spreading, and blood vessel wall stability. Circ Res. 2008;102:562-570.
19. David G, Bai XM, Van der Schueren B, Cassiman JJ, Van den Berghe H. Developmental changes in heparan sulfate expression: in situ detection with mAbs. J Cell Biol. 1992;119:961-975.
20. Ozerdem U, Grako KA, Dahlin-Huppe K, Monosov E, Stallcup WB. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev Dyn. 2001;222:218-227. (Pubitemid 32937594)
21. Brachtendorf G, Kuhn A, Samulowitz U, et al. Early expression of endomucin on endothelium of the mouse embryo and on putative hematopoietic clusters in the dorsal aorta. Dev Dyn. 2001;222:410-419. (Pubitemid 33042140)
22. Olivey HE, Compton LA, Barnett JV. Coronary vessel development: the epicardium delivers. Trends Cardiovasc Med. 2004;14:247-251.
23. Banerji S, Ni J, Wang SX, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol. 1999;144:789-801. (Pubitemid 29234556)
24. Baluk P, Lee CG, Link H, et al. Regulated angiogenesis and vascular regression in mice overexpressing vascular endothelial growth factor in airways. Am J Pathol. 2004;165:1071-1085. (Pubitemid 39297715)
25. Phng LK, Potente M, Leslie JD, et al. Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev Cell. 2009;16:70-82.
26. Enge M, Bjarnegard M, Gerhardt H, et al. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J. 2002;21:4307-4316. (Pubitemid 34898182)
27. Hammes HP, Lin J, Renner O, et al. Pericytes and the pathogenesis of diabetic retinopathy. Diabetes. 2002;51:3107-3112.
28. Hammes HP, Lin J, Wagner P, et al. Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes. 2004;53:1104-1110. (Pubitemid 38436625)
29. Jakobsson L, Kreuger J, Holmborn K, et al. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev Cell. 2006;10:625-634.
30. Han C, Belenkaya TY, Khodoun M, Tauchi M, Lin X, Lin X. Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development. 2004;131:1563-1575. (Pubitemid 38559283)
31. Chen Q, Sivakumar P, Barley C, et al. Potential role for heparan sulfate proteoglycans in regulation of transforming growth factor-beta (TGF-beta) by modulating assembly of latent TGF-beta-binding protein-1. J Biol Chem. 2007;282:26418-26430. (Pubitemid 47443781)
32. Eickelberg O, Centrella M, Reiss M, Kashgarian M, Wells RG. Betaglycan inhibits TGF-beta signaling by preventing type I-type II receptor complex formation: glycosaminoglycan modifications alter betaglycan function. J Biol Chem. 2002;277:823-829. (Pubitemid 34952123)
33. Rider CC. Heparin/heparan sulphate binding in the TGF-beta cytokine superfamily. Biochem Soc Trans. 2006;34:458-460.
34. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol. 1998;141:805-814 [erratum appears in J Cell Biol. 1998;141:1287].
35. Chakravarti R, Sapountzi V, Adams JC. Functional role of syndecan-1 cytoplasmic V region in lamellipodial spreading, actin bundling, and cell migration. Mol Biol Cell. 2005;16:3678-3691. (Pubitemid 41077078)
36. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005;97:512-523.
37. Etchevers HC, Vincent C, Le Douarin NM, Couly GF. The cephalic neural crest provides pericytes and smooth muscle cells to all blood vessels of the face and forebrain. Development. 2001;128:1059-1068. (Pubitemid 32401421)
38. Sato Y, Tsuboi R, Lyons R, Moses H, Rifkin DB. Characterization of the activation of latent TGF-beta by co-cultures of endothelial cells and pericytes or smooth muscle cells: a self-regulating system. J Cell Biol. 1990;111:757-763. (Pubitemid 20239886)
39. Goumans MJ, Mummery C. Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int J Dev Biol. 2000;44:253-265. (Pubitemid 30368069)
40. Fernandez-L A, Sanz-Rodriguez F, Blanco FJ, Bernabeu C, Botella LM. Hereditary hemorrhagic telangiectasia, a vascular dysplasia affecting the TGF-beta signaling pathway. Clin Med Res. 2006;4:66-78.
41. Vardouli L, Vasilaki E, Papadimitriou E, Kardassis D, Stournaras C. A novel mechanism of TGFbeta-induced actin reorganization mediated by Smad proteins and Rho GTPases. FEBS J. 2008;275:4074-4087.