Angiogenic modulators in valve development and disease: Does valvular disease recapitulate developmental signaling pathways?

Current Opinion in Cardiology

Volumn 19, Issue 2, 2004, Pages 140-146

  Shworak, Nicholas W ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Heart valvular development; Heart valvular disease

Indexed keywords

ANGIOGENIC FACTOR; CANCER GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; FIBROBLAST GROWTH FACTOR 4; GELATINASE A; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; SEROTONIN; TENASCIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANGIOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSFORMATION; DISEASE PREDISPOSITION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GENE EXPRESSION; INFLAMMATORY CELL; MESENCHYME CELL; MYOFIBROBLAST; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; VALVULAR HEART DISEASE;

ADULT; CELL DIFFERENTIATION; ENDOTHELIUM, VASCULAR; EPIDERMAL GROWTH FACTOR; EPITHELIUM; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTORS; HEART VALVE DISEASES; HEART VALVES; HUMANS; HYALURONIC ACID; MESODERM; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 1642339705     PISSN: 02684705     EISSN: None     Source Type: Journal    
DOI: 10.1097/00001573-200403000-00013     Document Type: Review

References (56)

1. McDonald PC, Wilson JE, Gao M, et al.: Quantitative analysis of human heart valves: does anorexigen exposure produce a distinctive morphological lesion? Cardiovasc Pathol 2002, 11:251-262. The authors use a novel quantitative analysis of digitalized histology to evaluate whether anorexigen valvular lesions are morphologically distinct entities.
2. Soini Y, Salo T, Satta J: Angiogenesis is involved in the pathogenesis of non-rheumatic aortic valve stenosis. Hum Pathol 2003, 34:756-763. This article employs immunohistochemical analysis of angiogenic modulators, in conjunction with vessel counts, to address mechanistic aspects. An interesting discussion of the potential role of angiogenesis in disease progression is provided.
3. Weind KL, Ellis CG, Boughner DR: Aortic valve cusp vessel density: relationship with tissue thickness. J Thorac Cardiovasc Surg 2002, 123:333-340.
4. Simula DV, Edwards WD, Tazelaar HD, et al.: Surgical pathology of carcinoid heart disease: a study of 39 valves from 75 patients spanning 20 years. Mayo Clin Proc 2002, 77:139-147.
5. Owens GK: Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 1995, 75:487-517.
6. Chien R: Signaling mechanisms for the activation of an embryonic gene program during the hypertrophy of cardiac ventricular muscle. Basic Res Cardiol 1992, 87(suppl 2):49-58.
7. Durbin AD, Gotlieb AI: Advances towards understanding heart valve response to injury. Cardiovasc Pathol 2002, 11:69-77. In this excellent review, the authors summarize the known molecular processes of valvular interstitial cells from the perspective that valvular dysfunction stems from an interstitial cell mediated response to injury.
8. Schroeder JA, Jackson LF, Lee DC, et al.: Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. J Mol Med 2003, 81:392-403. This comprehensive review explains how the extracellular matrix components actively participate in the molecular mechanisms governing heart valve formation. It covers a large number of effectors that control valvulogenesis.
9. Damert A, Miquerol L, Gertsenstein M, et al.: Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 2002, 129:1881-1892.
10. Miquerol L, Langille BL, Nagy A: Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 2000, 127:3941-3946.
11. Carmeliet P, Ferreira V, Breier G, et al.: Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
12. Dor Y, Camenisch TD, Itin A, et al.: A novel role for VEGF in endocardial cushion formation and its potential contribution to congenital heart defects. Development 2001, 128:1531-1538.
13. Enciso JM, Gratzinger D, Camenisch TD, et al.: Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J Cell Biol 2003, 160:605-615. This clever article describes the mechanisms by which hyperglycemic inhibition of VEGF-A prevents EMT. A comparable mechanism might be involved in cardiac congenital malformations associated with maternal diabetes.
14. Dor Y, Klewer SE, McDonald JA, et al.: VEGF modulates early heart valve formation. Anat Rec 2003, 271A:202-208. This paper demonstrates a second role for VEGF-A in EMT.
15. Rissanen TT, Markkanen JE, Arve K, et al.: Fibroblast growth factor 4 induces vascular permeability, angiogenesis and arteriogenesis in a rabbit hindlimb ischemia model. FASEB J 2003, 17:100-102. This preclinical study evaluates the revascularization efficacy of FGF-4 in a model of peripheral vascular disease.
16. Sugi Y, Ito N, Szebenyi G, et al.: Fibroblast growth factor (FGF)-4 can induce proliferation of cardiac cushion mesenchymal cells during early valve leaflet formation. Dev Biol 2003, 258:252-263. This developmental study using chick embryos implicates FGF-4 in the proliferative expansion phase of valvulogenesis.
17. Feldman B, Poueymirou W, Papaioannou VE, et al.: Requirement of FGF-4 for postimplantation mouse development. Science 1995, 267:246-249.
18. Deroanne CF, Hajitou A, Calberg-Bacq CM, et al.: Angiogenesis by fibroblast growth factor 4 is mediated through an autocrine up-regulation of vascular endothelial growth factor expression. Cancer Res 1997, 57:5590-5597.
19. Raab G, Klagsbrun M: Heparin-binding EGF-like growth factor. Biochim Biophys Acta 1997, 1333:F179-F199.
20. Riese DJ 2nd, Stern DF: Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 1998, 20:41-48.
21. Lee DC, Sunnarborg SW, Hinkle CL, et al.: TACE/ADAM17 processing of EGFR ligands indicates a role as a physiological convertase. Ann N Y Acad Sci 2003, 995:22-38. This review describes the evidence that TACE is a convertase that can process multiple ligands for EGFR.
22. Sunnarborg SW, Hinkle CL, Stevenson M, et al.: Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J Biol Chem 2002, 277:12838-12845.
23. Jackson LF, Qiu TH, Sunnarborg SW, et al.: Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling. EMBO J 2003, 22:2704-2716. This magnificent paper uses multiple genetically engineered mice to elucidate the mechanistic roll of HB-EGF in embryonic valvular remodeling. The role in adult dilated cardiomyopathy is also briefly addressed.
24. -/- adult mice, which develop a dilated cardiomyopathy.
25. Gassmann M, Casagranda F, Orioli D, et al.: Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 1995, 378:390-394.
26. Erickson SL, O'Shea KS, Ghaboosi N, et al.: ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 1997, 124:4999-5011.
27. Chen B, Bronson RT, Klaman LD, et al.: Mice mutant for Egfr and Shp2 have defective cardiac semilunar valvulogenesis. Nat Genet 2000, 24:296-299.
28. -/- mouse expressing human EGFR cDNA, which partially corrects the EGFR deficiency in a cell type-specific fashion.
29. Slevin M, Kumar S, Gaffney J: Angiogenic oligosaccharides of hyaluronan induce multiple signaling pathways affecting vascular endothelial cell mitogenic and wound healing responses. J Biol Chem 2002, 277:41046-41059. This paper elucidates the cell signaling pathways initiated by HA oligosaccharides to exert a proangiogenic effect.
30. Deed R, Rooney P, Kumar P, et al.: Early-response gene signalling is induced by angiogenic oligosaccharides of hyaluronan in endothelial cells. Inhibition by non-angiogenic, high-molecular-weight hyaluronan. Int J Cancer 1997, 71:251-256.
31. Camenisch TD, Spicer AP, Brehm-Gibson T, et al.: Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 2000, 106:349-360.
32. Mjaatvedt CH, Yamamura H, Capehart AA, et al.: The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev Bid 1998, 202:56-66.
33. Hurlstone AF, Haramis AP, Wienholds E, et al.: The Wnt/beta-catenin pathway regulates cardiac valve formation. Nature 2003, 425:633-637. This superb article uses chemical mutagenesis of zebrafish to demonstrate a novel role for the Wnt canonical signaling pathway.
34. Goodwin AM, D'Amore PA: Wnt signaling in the vasculature. Angiogenesis 2002, 5:1-9.
35. Camenisch TD, Schroeder JA, Bradley J, et al.: Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nat Med 2002, 8:850-855. This landmark article demonstrates that HA is not simply a structural component of the extracellular matrix but can also modulate cell-signaling activities.
36. Taylor PM, Batten P, Brand NJ, et al.: The cardiac valve interstitial cell. Int J Biochem Cell Biol 2003, 35:113-118. This review describes phenotypic and molecular properties of interstitial cells and then addresses their role in valvular disease.
37. Leask RL, Jain N, Butany J: Endothelium and valvular diseases of the heart. Microsc Res Tech 2003, 60:129-137. This comprehensive review evaluates the role of endothelial dysfunction in several varieties of valvular disease. This is a well-written and well-illustrated review.
38. Gotlieb AI, Rosenthal A, Kazemian P: Fibroblast growth factor 2 regulation of mitral valve interstitial cell repair in vitro. J Thorac Cardiovasc Surg 2002, 124:591-597. This article applies an in vitro model of wound healing to evaluate molecular changes that occur in interstitial cells during the response to injury.
39. Choy M, Oltjen SL, Otani YS, et al.: Fibroblast growth factor-2 stimulates embryonic cardiac mesenchymal cell proliferation. Dev Dyn 1996, 206:193-200.
40. Watanabe C, Sugiura M, Ohkawa S, et al.: Pathology and histochemistry of mitral valve prolapse. J Cardiol 1993, 23:69-77.
41. Castagnaro M, Amedeo S, Bertolotto A, et al.: Morphological and biochemical investigations of mitral valve endocardiosis in pigs. Res Vet Sci 1997, 62:121-125.
42. Colvee E, Hurle JM: Maturation of the extracellular material of the semilunar heart values in the mouse. A histochemical analysis of collagen and mucopolysaccharides. Anat Embryol (Berl) 1981, 162:343-352.
43. Grande-Allen KJ, Griffin BP, Ratliff NB, et al.: Glycosaminoglycan profiles of myxomatous mitral leaflets and chordae parallel the severity of mechanical alterations. J Am Coll Cardiol 2003, 42:271-277. This article employs biochemical analyses of major forms of glycosaminoglycan to provide a basis for the mechanical and echocardiographic distinctions between unileaflet mitral prolapse and bileaflet prolapse.
44. Paranya G, Vineberg S, Dvorin E, et al.: Aortic valve endothelial cells undergo transforming growth factor-beta-mediated and non-transforming growth factor-beta-mediated transdifferentiation in vitro. Am J Pathol 2001, 159:1335-1343.
45. Dvorin EL, Wylie-Sears J, Kaushal S, et al.: Quantitative evaluation of endothelial progenitors and cardiac valve endothelial cells: proliferation and differentiation on poly-glycolic acid/poly-4-hydroxybutyrate scaffold in response to vascular endothelial growth factor and transforming growth factor beta1. Tissue Eng 2003, 9:487-493. This article provides a means to evaluate potential components of a bionic prosthetic valve to maintain appropriate endothelial and interstitial cell phenotypes.
46. Moller JE, Connolly HM, Rubin J, et al.: Factors associated with progression of carcinoid heart disease. N Engl J Med 2003, 348:1005-1015. This retrospective study provides echocardiographic and biochemical standards to evaluate the progression of carcinoid heart disease.
47. Jian B, Xu J, Connolly J, et al.: Serotonin mechanisms in heart valve disease I: serotonin-induced up-regulation of transforming growth factor-beta1 via G-protein signal transduction in aortic valve interstitial cells. Am J Pathol 2002, 161:2111-2121. In this elegant study, immunohistopathology is combined with cell culture to reveal a likely signaling cascade involved in carcinoid valve disease.
48. Xu J, Jian B, Chu R, et al.: Serotonin mechanisms in heart valve disease II: the 5-HT2 receptor and its signaling pathway in aortic valve interstitial cells. Am J Pathol 2002, 161:2209-2218. This follow-up study further explores the detailed nature of serotonin signaling in interstitial cells.
49. Jian B, Narula N, Li QY, et al.: Progression of aortic valve stenosis: TGF-beta1 is present in calcified aortic valve cusps and promotes aortic valve interstitial cell calcification via apoptosis. Ann Thorac Surg 2003, 75:457-465. Again, Jian et al. have elegantly combined immunohistopathology with cell culture to define a critical signaling pathway in valve disease. This study provides the foundations for future medical treatment of a present-day surgical disease.
50. Kim KM. Apoptosis and calcification. Scanning Microsc 1995; 9:1137-1175; discussion 1175-1178.
51. Crossin KL, Hoffman S: Expression of adhesion molecules during the formation and differentiation of the avian endocardial cushion tissue. Dev Biol 1991, 145:277-286.
52. Jian B, Jones PL, Li Q, et al.: Matrix metalloproteinase-2 is associated with tenascin-C in calcific aortic stenosis. Am J Pathol 2001, 159:321-327.
53. Satta J, Melkko J, Pollanen R, et al.: Progression of human aortic valve stenosis is associated with tenascin-C expression. J Am Coll Cardiol 2002, 39:96-101. This histopathologic analysis evaluates the extent of tenascin-C expression compared with clinic severity.
54. Li QY, Jones PL, Lafferty RP, et al.: Thymosin beta4 regulation, expression and function in aortic valve interstitial cells. J Heart Valve Dis 2002, 11:726-735. This molecular analysis provides a mechanism for the coexpression of tenascin-C and MMP-2 in calcific leaflets.
55. Satta J, Oiva J, Salo T, et al.: Evidence for an altered balance between matrix metalloproteinase-9 and its inhibitors in calcific aortic stenosis. Ann Thorac Surg 2003, 76:681-688. This histopathologic analysis evaluates the expression of active MMPs and their inhibitors. Their striking finding is that reduced inhibitor activity may be a major contributor to high MMP-9 activity in calcific leaflets.
56. Stefanidakis M, Bjorklund M, Ihanus E, et al.: Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte beta 2 integrins. J Biol Chem 2003, 278:34674-34684. This article employs a phage display search with cell biology to define a novel role for pro-MMPs.