A central function for perlecan in skeletal muscle and cardiovascular development

Journal of Cell Biology

Volumn 181, Issue 2, 2008, Pages 381-394

  Zoeller, Jason J ^a,b   McQuillan, Angela ^a,b   Whitelock, John ^d   Ho, Shiu Ying ^a,c   Iozzo, Renato V ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOREPELLIN; PEPTIDE FRAGMENT; PERLECAN; UNCLASSIFIED DRUG; ANTISENSE OLIGONUCLEOTIDE; PRIMER DNA; PROTEOHEPARAN SULFATE;

ACTIN FILAMENT; ANGIOGENESIS; ARTICLE; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; MYOPATHY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SARCOMERE; SKELETAL MUSCLE; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; BLOOD VESSEL; DRUG EFFECT; FETUS HEART; GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT; VASCULARIZATION;

ANIMALIA; DANIO RERIO; MAMMALIA;

ANIMALS; BLOOD VESSELS; DNA PRIMERS; EMBRYO, NONMAMMALIAN; FETAL HEART; HEPARAN SULFATE PROTEOGLYCANS; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGONUCLEOTIDES, ANTISENSE; ZEBRAFISH;

EID: 42449140214     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200708022     Document Type: Article

References (68)

1. Arikawa-Hirasawa, E., E. Watanabe, H. Takami, J.R. Hassell, and Y. Yamada. 1999. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 23:354-358.
2. Arikawa-Hirasawa, E., S.G. Rossi, R.L. Rotundo, and Y. Yamada. 2002. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat. Neurosci. 5:119-123.
3. Aviezer, D., D. Hecht, M. Safran, M. Eisinger, G. David, and A. Yayon. 1994. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell. 79: 1005-1013.
4. Aviezer, D., R.V. Iozzo, D.M. Noonan, and A. Yayon. 1997. Suppression of autocrine and paracrine functions of basic fibroblast growth factor by stable expression of perlecan antisense cDNA. Mol. Cell. Biol. 17:1938-1946.
5. Bassett, D.I., and P.D. Currie. 2003. The zebrafish as a model for muscular dystrophy and congenital myopathy. Hum. Mol. Genet. 12:R265-R270.
6. Bassett, D.I., R.J. Bryson-Richardson, D.F. Daggett, P. Gautier, D.G. Keenan, and P.D. Currie. 2003. Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development. 130:5851-5860.
7. Behra, M., X. Cousin, C. Bertrand, J.-L. Vonesch, D. Biellmann, A. Chatonnet, and U. Strähle. 2002. Acetylcholinesterase is required for neuronal and muscular development in the zebrafish embryo. Nat. Neurosci. 5:111-118.
8. Bishop, J.R., M. Schuksz, and J.D. Esko. 2007. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature. 446:1030-1037.
9. Bix, G., J. Fu, E. Gonzalez, L. Macro, A. Barker, S. Campbell, M.M. Zutter, S.A. Santoro, J.K. Kim, M. Höök, et al. 2004. Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through the α2β1 integrin. J. Cell Biol. 166:97-109.
10. Bix, G., R. Castello, M. Burrows, J.J. Zoeller, M. Weech, R.A. Iozzo, C. Cardi, M.T. Thakur, C.A. Barker, K.C. Camphausen, and R.V. Iozzo. 2006. Endorepellin in vivo: targeting the tumor vasculature and retarding cancer growth and metabolism. J. Natl. Cancer Inst. 98:1634-1646.
11. Bix, G., R.A. Iozzo, B. Woodall, M. Burrows, A. McQuillan, S. Campbell, G.B. Fields, and R.V. Iozzo. 2007. Endorepellin, the C-terminal angiostatic module of perlecan, enhances collagen-platelet responses via the α2β1 integrin receptor. Blood. 109:3745-3748.
12. Carmeliet, P. 2005. Angiogenesis in life, disease and medicine. Nature. 438:932-936.
13. Childs, S., J.-N. Chen, D.M. Garrity, and M.C. Fishman. 2002. Patterning of angiogenesis in the zebrafish embryo. Development. 129:973-982.
14. Costell, M., E. Gustafsson, A. Aszódi, M. Mörgelin, W. Bloch, E. Hunziker, K. Addicks, R. Timpl, and R. Fässler. 1999. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 147:1109-1122.
15. Costell, M., R. Carmona, E. Gustafsson, M. González-Iriarte, R. Fässler, and R. Munoz-Chápuli. 2002. Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecan-null mice. Circ. Res. 91:158-164.
16. Covassin, L.D., J.A. Villefranc, M.C. Kacergis, B.M. Weinstein, and N.D. Lawson. 2006. Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc. Natl. Acad. Sci. USA. 103:6554-6559.
17. Cross, L.M., M.A. Cook, S. Lin, J.-N. Chen, and A.L. Rubinstein. 2003. Rapid analysis of angiogenic drugs in a live fluorescent zebrafish assay. Arterioscler. Thromb. Vasc. Biol. 23:911-912.
18. Datta, M.W., A.M. Hernandez, M.J. Schlicht, A.J. Kahler, A.M. DeGueme, R. Dhir, R.B. Shah, C. Farach-Carson, A. Barrett, and S. Datta. 2006a. Perlecan, a candidate gene for the CAPB locus, regulates prostate cancer cell growth via the Sonic Hedgehog pathway. Mol. Cancer. 5:9.
19. Datta, S., M. Pierce, and M.W. Datta. 2006b. Perlecan signaling: helping hedgehog stimulate prostate cancer growth. Int. J. Biochem. Cell Biol. 38:1855-1861.
20. Drapeau, P., R.R. Buss, D.W. Ali, P. Legendre, and R.L. Rotundo. 2001. Limits to the development of fast neuromuscular transmission in zebrafish. J. Neurophysiol. 86:2951-2956.
21. Fuki, I.V., R.V. Iozzo, and K.J. Williams. 2000. Perlecan heparan sulfate proteoglycan. A novel receptor that mediates a distinct pathway for ligand catabolism. J. Biol. Chem. 275:25742-25750.
22. Gering, M., and R. Patient. 2005. Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev. Cell. 8:389-400.
23. Gonzalez, E.M., C.C. Reed, G. Bix, J. Fu, Y. Zhang, B. Gopalakrishnan, D.S. Greenspan, and R.V. Iozzo. 2005. BMP-1/Tolloid-like metalloproteases process endorepellin, the angiostatic C-terminal fragment of perlecan. J. Biol. Chem. 280:7080-7087.
24. González-Iriarte, M., R. Carmona, J.M. Pérez-Pomares, D. Macías, M. Costell, and R. Munoz-Chápuli. 2003. Development of the coronary arteries in a murine model of transposition of great arteries. J. Mol. Cell. Cardiol. 35:795-802.
25. Granato, M., F.J.M. van Eeden, U. Schach, T. Trowe, M. Brand, M. Furutani-Seiki, P. Haffter, M. Hammerschmidt, C.-P. Heisenberg, Y.-J. Jiang, et al. 1996. Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development. 123:399-413.
26. Guyon, J.R., A.N. Mosley, S.J. Jun, F. Montanaro, L.S. Steffen, Y. Zhou, V. Nigro, L.I. Zon, and L.M. Kunkel. 2005. δ-sarcoglycan is required for early zebrafish muscle organization. Exp. Cell Res. 304:105-115.
27. Guyon, J.R., L.S. Steffen, M.H. Howell, T.J. Pusack, C. Lawrence, and L.M. Kunkel. 2007. Modeling human muscle disease in zebrafish. Biochim. Biophys. Acta. 1772:205-215.
28. Handler, M., P.D. Yurchenco, and R.V. Iozzo. 1997. Developmental expression of perlecan during murine embryogenesis. Dev. Dyn. 210:130-145.
29. Hassell, J, Y. Yamada, and E. Arikawa-Hirasawa. 2 002. Role of perlecan in skeletal development and diseases. Glycoconj. J. 19:263-267.
30. Iozzo, R.V. 1998. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67:609-652.
31. Iozzo, R.V. 2005. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 6:646-656.
32. Iozzo, R.V., and J.D. San Antonio. 2001. Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J. Clin. Invest. 108:349-355.
33. Isogai, S., M. Horiguchi, and B.M. Weinstein. 2001. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230:278-301.
34. Isogai, S., N.D. Lawson, S. Torrealday, M. Horiguchi, and B.M. Weinstein. 2003. Angiogenic network formation in the developing vertebrate trunk. Development. 130:5281-5290.
35. Kanagawa, M., D.E. Michele, J.S. Satz, R. Barresi, H. Kusano, T. Sasaki, R. Timpl, M.D. Henry, and K.P. Campbell. 2005. Disruption of perlecan binding and matrix assembly by post-translational or genetic disruption of dystroglycan function. FEBS Lett. 579:4792-4796.
36. Knox, S.M., and J.M. Whitelock. 2006. Perlecan: how does one molecule do so many things? Cell. Mol. Life Sci. 63:2435-2445.
37. Kunkel, L.M., E. Bachrach, R.R. Bennett, J. Guyon, and L. Steffen. 2006. Diagnosis and cell-based therapy for duchenne muscular dystrophy in humans, mice, and zebrafish. J. Hum. Genet. 51:397-406.
38. Lawson, N.D., and B.M. Weinstein. 2002. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248:307-318.
39. Lawson, N.D., N. Scheer, V.N. Pham, C.-H. Kim, A.B. Chitnis, J.A. Campos-Ortega, and B.M. Weinstein. 2001. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development. 128:3675-3683.
40. Lawson, N.D., A.M. Vogel, and B.M. Weinstein. 2002. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell. 3:127-136.
41. Lindner, J.R., P.R. Hillman, A.L. Barrett, M.C. Jackson, T.L. Perry, Y. Park, and S. Datta. 2007. The Drosophila Perlecan gene trol regulates multiple signaling pathways in different developmental contexts. BMC Dev. Biol. 7:121.
42. Mathiak, M., C. Yenisey, D.S. Grant, B. Sharma, and R.V. Iozzo. 1997. A role for perlecan in the suppression of growth and invasion in fibrosarcoma cells. Cancer Res. 57:2130-2136.
43. Mongiat, M., S. Sweeney, J.D. San Antonio, J. Fu, and R.V. Iozzo. 2003. Endorepellin, a novel inhibitor of angiogenesis derived from the C terminus of perlecan. J. Biol. Chem. 278:4238-4249.
44. Nasevicius, A., and S.C. Ekker. 2000. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26:216-220.
45. Nasevicius, A., J. Larson, and S.C. Ekker. 2000. Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant. Yeast. 17:294-301.
46. Park, Y., C. Rangel, M.M. Reynolds, M.C. Caldwell, M. Johns, M. Nayak, C.J.R. Welsh, S. McDermott, and S. Datta. 2003. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev. Biol. 253:247-257.
47. Parsons, M.J., I. Campos, E.M.A. Hirst, and D.L. Stemple. 2002. Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development. 129:3505-3512.
48. Peng, H.B., A.A. Ali, D.F. Daggett, H. Rauvala, J.R. Hassell, and N.R. Smalheiser. 1998. The relationship between perlecan and dystroglycan and its implication in the formation of the neuromuscular junction. Cell Adhes. Commun. 5:475-489.
49. Peng, H.B., H. Xie, S.G. Rossi, and R.L. Rotundo. 1999. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J. Cell Biol. 145:911-921.
50. Robu, M.E., J.D. Larson, A. Nasevicius, S. Beiraghi, C. Brenner, S.A. Farber, and S.C. Ekker. 2007. p53 activation by knockdown technologies. PLoS Genet. 3:e78.
51. Rodgers, K.D., T. Sasaki, A. Aszodi, and O. Jacenko. 2007. Reduced perlecan in mice results in chondrodysplasia resembling Schwartz-Jampel syndrome. Hum. Mol. Genet. 16:515-528.
52. Rossi, M., H. Morita, R. Sormunen, S. Airenne, M. Kreivi, L. Wang, N. Fukai, B.R. Olsen, K. Tryggvason, and R. Soininen. 2003. Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22:236-245.
53. Rotundo, R.L. 2003. Expression and localization of acetylcholinesterase at the neuromuscular junction. J. Neurocytol. 32:743-766.
54. Schneider, M., A.A. Khalil, J. Poulton, C. Castillejo-Lopez, D. Egger-Adam, A. Wodarz, W.-M. Deng, and S. Baumgartner. 2006. Perlecan and dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization. Development. 133:3805-3815.
55. Sharma, B., M. Handler, I. Eichstetter, J. Whitelock, M.A. Nugent, and R.V. Iozzo. 1998. Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo. J. Clin. Invest. 102:1599-1608.
56. Smirnov, S.P., P. Barzaghi, K.K. McKee, M.A. Ruegg, and P.D. Yurchenco. 2005. Conjugation of LG domains of agrins and perlecan to polymerizing laminin-2 promotes acetylcholine receptor clustering. J. Biol. Chem. 280:41449-41457.
57. Stum, M., C.-S. Davoine, S. Vicart, L. Guillot-Noël, H. Topaloglu, F.J. Carod-Artal, H. Kayserili, F. Hentati, L. Merlini, J.A. Urtizberea, et al. 2006. Spectrum of HSPG2 (perlecan) mutations in patients with schwartz-jampel syndrome. Hum. Mutat. 27:1082-1091.
58. Talts, J.F., Z. Andac, W. Göhring, A. Brancaccio, and R. Timpl. 1999. Binding of the G domains of laminin α1 and α2 chains and perlecan to heparin, sulfatides, α-dystroglycan and several extracellular matrix proteins. EMBO J. 18:863-870.
59. Tran, P.-K., K. Tran-Lundmark, R. Soininen, K. Tryggvason, J. Thyberg, and U. Hedin. 2004. Increased intimal hyperplasia and smooth muscle cell proliferation in transgenic mice with heparan sulfate-deficient perlecan. Circ. Res. 94:550-558.
60. Villar, M.J., J.R. Hassell, and E. Brandan. 1999. Interaction of skeletal muscle cells with collagen type IV is mediated by perlecan associated with the cell surface. J. Cell. Biochem. 75:665-674.
61. Vokes, S.A., T.A. Yatskievych, R.L. Heimark, J. McMahon, A.P. McMahon, P.B. Antin, and P.A. Krieg. 2004. Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development. 131:4371-4380.
62. Wang, H., K. Julenius, J. Hryhorenko, and F.K. Hagen. 2007. Systematic analysis of proteoglycan modification sites in Caenorhabditis elegans by scanning mutagenesis. J. Biol. Chem. 282:14586-14597.
63. Whitelock, J.M., and R.V. Iozzo. 2002. Isolation and purification of proteoglycans. In Methods in Cell-Matrix Adhesion. J.C. Adams, editor. Academic Press, San Diego. 53-67.
64. Whitelock, J.M., and R.V. Iozzo. 2005. Heparan sulfate: a complex polymer charged with biological activity. Chem. Rev. 105:2745-2764.
65. Whitelock, J.M., L.D. Graham, J. Melrose, A.D. Murdoch, R.V. Iozzo, and P.A. Underwood. 1999. Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol. 18:163-178.
66. Woodall, B.P., A. Nyström, R.A. Iozzo, J.A. Eble, S. Niland, T. Krieg, B. Eckes, A. Pozzi, and R.V. Iozzo. 2008. Integrin α2β1 is the required receptor for endorepellin angiostatic activity. J. Biol. Chem. 283:2335-2343.
67. Zhou, Z., J. Wang, R. Cao, H. Morita, R. Soininen, K.M. Chan, B. Liu, Y. Cao, and K. Tryggvason. 2004. Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice. Cancer Res. 64:4699-4702.
68. Zoeller, J.J., and R.V. Iozzo. 2008. Proteomic profiling of endorepellin angiostatic activity on human endothelial cells. Proteome Sci. 6:7.