Control of organization and function of muscle and tendon by thrombospondin-4

Matrix Biology

Volumn 37, Issue , 2014, Pages 35-48

  Frolova, Ella G ^a   Drazba, Judith ^a   Krukovets, Irene ^a   Kostenko, Volodymyr ^a   Blech, Lauren ^a   Harry, Christy ^a   Vasanji, Amit ^a   Drumm, Carla ^a   Sul, Pavel ^a   Jenniskens, Guido J ^b,c   Plow, Edward F ^a   Stenina Adognravi, Olga ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ModiQuest Research BV   (Netherlands)

Author keywords

Glycosaminoglycans; Skeletal muscle; Tendon; Thrombospondin 4

Indexed keywords

CARTILAGE OLIGOMERIC MATRIX PROTEIN; COLLAGEN; GLYCOSAMINOGLYCAN; LIPOPROTEIN LIPASE; THROMBOSPONDIN; THROMBOSPONDIN 3; THROMBOSPONDIN 4; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; HEPARAN SULFATE; PRIMER DNA; SCLEROPROTEIN;

AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FEMALE; GRIP STRENGTH; IMMUNOHISTOCHEMISTRY; MALE; MICROVASCULATURE; MOUSE; MUSCLE FUNCTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SKELETAL MUSCLE; SOLEUS MUSCLE; TENDON; ANIMAL; CONFOCAL MICROSCOPY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUSCLE STRENGTH; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; COLLAGEN; DNA PRIMERS; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX PROTEINS; GLYCOSAMINOGLYCANS; HEPARITIN SULFATE; IMMUNOHISTOCHEMISTRY; LIPOPROTEINS, VLDL; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MUSCLE STRENGTH; MUSCLE, SKELETAL; TENDONS; THROMBOSPONDINS;

EID: 84908350506     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.02.003     Document Type: Article

References (76)

1. Adams J.C. Thrombospondins: multifunctional regulators of cell interactions. Annu. Rev. Cell Dev. Biol. 2001, 17:25-51.
2. Adams J.C. Functions of the conserved thrombospondin carboxy-terminal cassette in cell-extracellular matrix interactions and signaling. Int. J. Biochem. Cell Biol. 2004, 36:1102-1114.
3. Adams J.C., Lawler J. Cell-type specific adhesive interactions of skeletal myoblasts with thrombospondin-1. Mol. Biol. Cell 1994, 5:423-437.
4. Adams J.C., Lawler J. The thrombospondins. Int. J. Biochem. Cell Biol. 2004, 36:961-968.
5. Ameye L., Aria D., Jepsen K., Oldberg A., Xu T., Young M.F. Abnormal collagen fibrils in tendons of biglycan/fibromodulin-deficient mice lead to gait impairment, ectopic ossification, and osteoarthritis. FASEB J. 2002, 16:673-680.
6. Arber S., Caroni P. Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J. Cell Biol. 1995, 131:1083-1094.
7. Berryman D.E., Bensadoun A. Heparan sulfate proteoglycans are primarily responsible for the maintenance of enzyme activity, binding, and degradation of lipoprotein lipase in Chinese hamster ovary cells. J. Biol. Chem. 1995, 270:24525-24531.
8. Bilandzic M., Stenvers K.L. Betaglycan: a multifunctional accessory. Mol. Cell. Endocrinol. 2011, 339:180-189.
9. Bornstein P. Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J. Cell Biol. 1995, 130:503-506.
10. Bornstein P. Thrombospondins as matricellular modulators of cell function. J. Clin. Invest. 2001, 107:929-934.
11. Castellot J.J., Addonizio M.L., Rosenberg R., Karnovsky M.J. Cultured endothelial cells produce a heparin-like inhibitor of smooth muscle cell growth. J. Cell Biol. 1981, 90:372-379.
12. Chen H., Herndon M.E., Lawler J. The cell biology of thrombospondin-1. Matrix Biol. 2000, 19:597-614.
13. Chen F.H., Herndon M.E., Patel N., Hecht J.T., Tuan R.S., Lawler J. Interaction of cartilage oligomeric matrix protein/thrombospondin 5 with aggrecan. J. Biol. Chem. 2007, 282:24591-24598.
14. Cingolani O.H., Kirk J.A., Seo K., Koitabashi N., Lee D.I., Ramirez-Correa G., Bedja D., Barth A.S., Moens A.L., Kass D.A. Thrombospondin-4 is required for stretch-mediated contractility augmentation in cardiac muscle. Circ. Res. 2011, 109:1410-1414.
15. Corsi A., Xu T., Chen X.D., Boyde A., Liang J., Mankani M., Sommer B., Iozzo R.V., Eichstetter I., Robey P.G., Bianco P., Young M.F. Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J. Bone Miner. Res. 2002, 17:1180-1189.
16. Cui J., Randell E., Renouf J., Sun G., Han F.Y., Younghusband B., Xie Y.G. Gender dependent association of thrombospondin-4 A387P polymorphism with myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 2004, 24:e183-e184.
17. Cui J., Randell E., Renouf J., Sun G., Green R., Han F.Y., Xie Y.G. Thrombospondin-4 1186G>C (A387P) is a sex-dependent risk factor for myocardial infarction: a large replication study with increased sample size from the same population. Am. Heart J. 2006, 152(543):e541-e545.
18. De Agostini A.L., Lau H.K., Leone C., Youssoufian H., Rosenberg R.D. Cell mutants defective in synthesizing a heparan sulfate proteoglycan with regions of defined monosaccharide sequence. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:9784-9788.
19. Dennissen M.A., Jenniskens G.J., Pieffers M., Versteeg E.M., Petitou M., Veerkamp J.H., van Kuppevelt T.H. Large, tissue-regulated domain diversity of heparan sulfates demonstrated by phage display antibodies. J. Biol. Chem. 2002, 277:10982-10986.
20. Eisenberg S., Sehayek E., Olivecrona T., Vlodavsky I. Lipoprotein lipase enhances binding of lipoproteins to heparan sulfate on cell surfaces and extracellular matrix. J. Clin. Invest. 1992, 90:2013-2021.
21. Engel J. Role of oligomerization domains in thrombospondins and other extracellular matrix proteins. Int. J. Biochem. Cell Biol. 2004, 36:997-1004.
22. Ezura Y., Chakravarti S., Oldberg A., Chervoneva I., Birk D.E. Differential expression of lumican and fibromodulin regulate collagen fibrillogenesis in developing mouse tendons. J. Cell Biol. 2000, 151:779-788.
23. Frolova E.G., Pluskota E., Krukovets I., Burke T., Drumm C., Smith J.D., Blech L., Febbraio M., Bornstein P., Plow E.F., Stenina O.I. Thrombospondin-4 regulates vascular inflammation and atherogenesis. Circ. Res. 2010, 107:1313-1325.
24. Frolova E.G., Sopko N., Blech L., Popovic Z.B., Li J., Vasanji A., Drumm C., Krukovets I., Jain M.K., Penn M.S., Plow E.F., Stenina O.I. Thrombospondin-4 regulates fibrosis and remodeling of the myocardium in response to pressure overload. FASEB J. 2012, 26:2363-2373.
25. Fuki I.V., Blanchard N., Jin W., Marchadier D.H., Millar J.S., Glick J.M., Rader D.J. Endogenously produced endothelial lipase enhances binding and cellular processing of plasma lipoproteins via heparan sulfate proteoglycan-mediated pathway. J. Biol. Chem. 2003, 278:34331-34338.
26. Gatza C.E., Oh S.Y., Blobe G.C. Roles for the type III TGF-beta receptor in human cancer. Cell. Signal. 2010, 22:1163-1174.
27. Gilsohn E., Volk T. Slowdown promotes muscle integrity by modulating integrin-mediated adhesion at the myotendinous junction. Development 2010, 137:785-794.
28. Hankenson K.D., Hormuzdi S.G., Meganck J.A., Bornstein P. Mice with a disruption of the thrombospondin 3 gene differ in geometric and biomechanical properties of bone and have accelerated development of the femoral head. Mol. Cell. Biol. 2005, 25:5599-5606.
29. Hansen-Smith F., Banker K., Morris L., Joswiak G. Alternative histochemical markers for skeletal muscle capillaries: a statistical comparison among three muscles. Microvasc. Res. 1992, 44:112-116.
30. Hauser N., Paulsson M., Kale A.A., DiCesare P.E. Tendon extracellular matrix contains pentameric thrombospondin-4 (TSP-4). FEBS Lett. 1995, 368:307-310.
31. Hayashi K., Madri J.A., Yurchenco P.D. Endothelial cells interact with the core protein of basement membrane perlecan through beta 1 and beta 3 integrins: an adhesion modulated by glycosaminoglycan. J. Cell Biol. 1992, 119:945-959.
32. Hecht J.T., Deere M., Putnam E., Cole W., Vertel B., Chen H., Lawler J. Characterization of cartilage oligomeric matrix protein (COMP) in human normal and pseudoachondroplasia musculoskeletal tissues. Matrix Biol. 1998, 17:269-278.
33. Jenniskens G.J., Oosterhof A., Brandwijk R., Veerkamp J.H., van Kuppevelt T.H. Heparan sulfate heterogeneity in skeletal muscle basal lamina: demonstration by phage display-derived antibodies. J. Neurosci. 2000, 20:4099-4111.
34. Jenniskens G.J., Veerkamp J.H., van Kuppevelt T.H. Heparan sulfates in skeletal muscle development and physiology. J. Cell. Physiol. 2006, 206:283-294.
35. Jepsen K.J., Wu F., Peragallo J.H., Paul J., Roberts L., Ezura Y., Oldberg A., Birk D.E., Chakravarti S. A syndrome of joint laxity and impaired tendon integrity in lumican- and fibromodulin-deficient mice. J. Biol. Chem. 2002, 277:35532-35540.
36. Kannus P., Jozsa L., Jarvinen T.A., Jarvinen T.L., Kvist M., Natri A., Jarvinen M. Location and distribution of non-collagenous matrix proteins in musculoskeletal tissues of rat. Histochem. J. 1998, 30:799-810.
37. Kanwar Y.S., Farquhar M.G. Presence of heparan sulfate in the glomerular basement membrane. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:1303-1307.
38. Kato T.Y.A., Murase Y., Hirashiki A., Noda A., Yamada Y. Specific gene polymorphisms could be risk factors for coronary artery disease in individuals with or without hypertension. Circulation 2003, 108:IV-712. (Suppl.).
39. Kolset S.O., Salmivirta M. Cell surface heparan sulfate proteoglycans and lipoprotein metabolism. Cell. Mol. Life Sci. 1999, 56:857-870.
40. Kyriakides T.R., Zhu Y.H., Smith L.T., Bain S.D., Yang Z., Lin M.T., Danielson K.G., Iozzo R.V., LaMarca M., McKinney C.E., Ginns E.I., Bornstein P. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J. Cell Biol. 1998, 140:419-430.
41. Lawler J., Duquette M., Whittaker C.A., Adams J.C., McHenry K., DeSimone D.W. Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family. J. Cell Biol. 1993, 120:1059-1067.
42. Lawler J., Sunday M., Thibert V., Duquette M., George E.L., Rayburn H., Hynes R.O. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J. Clin. Invest. 1998, 101:982-992.
43. Lynch J.M., Maillet M., Vanhoutte D., Schloemer A., Sargent M.A., Blair N.S., Lynch K.A., Okada T., Aronow B.J., Osinska H., Prywes R., Lorenz J.N., Mori K., Lawler J., Robbins J., Molkentin J.D. A thrombospondin-dependent pathway for a protective ER stress response. Cell 2012, 149:1257-1268.
44. Mahabeleshwar G.H., Somanath P.R., Byzova T.V. Methods for isolation of endothelial and smooth muscle cells and in vitro proliferation assays. Methods Mol. Med. 2006, 129:197-208.
45. Marchant J.K., Hahn R.A., Linsenmayer T.F., Birk D.E. Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. J. Cell Biol. 1996, 135:1415-1426.
46. McCarthy J.J., Parker A., Salem R., Moliterno D.J., Wang Q., Plow E.F., Rao S., Shen G., Rogers W.J., Newby L.K., Cannata R., Glatt K., Topol E.J. Large scale association analysis for identification of genes underlying premature coronary heart disease: cumulative perspective from analysis of 111 candidate genes. J. Med. Genet. 2004, 41:334-341.
47. Misenheimer T.M., Mosher D.F. Biophysical characterization of the signature domains of thrombospondin-4 and thrombospondin-2. J. Biol. Chem. 2005, 280:41229-41235.
48. Misra K.B., Kim K.C., Cho S., Low M.G., Bensadoun A. Purification and characterization of adipocyte heparan sulfate proteoglycans with affinity for lipoprotein lipase. J. Biol. Chem. 1994, 269:23838-23844.
49. Mosher D.F., Adams J.C. Adhesion-modulating/matricellular ECM protein families: a structural, functional and evolutionary appraisal. Matrix Biol. 2012, 31:155-161.
50. Murphy-Ullrich J.E., Iozzo R.V. Thrombospondins in physiology and disease: new tricks for old dogs. Matrix Biol. 2012, 31:152-154.
51. Mustonen E., Aro J., Puhakka J., Ilves M., Soini Y., Leskinen H., Ruskoaho H., Rysa J. Thrombospondin-4 expression is rapidly upregulated by cardiac overload. Biochem. Biophys. Res. Commun. 2008, 373:186-191.
52. Naimy H., Leymarie N., Bowman M.J., Zaia J. Characterization of heparin oligosaccharides binding specifically to antithrombin III using mass spectrometry. Biochemistry 2008, 47:3155-3161.
53. Narouz-Ott L., Maurer P., Nitsche D.P., Smyth N., Paulsson M. Thrombospondin-4 binds specifically to both collagenous and non-collagenous extracellular matrix proteins via its C-terminal domains. J. Biol. Chem. 2000, 275:37110-37117.
54. Parthasarathy N., Goldberg I.J., Sivaram P., Mulloy B., Flory D.M., Wagner W.D. Oligosaccharide sequences of endothelial cell surface heparan sulfate proteoglycan with affinity for lipoprotein lipase. J. Biol. Chem. 1994, 269:22391-22396.
55. Riessen R., Fenchel M., Chen H., Axel D.I., Karsch K.R., Lawler J. Cartilage oligomeric matrix protein (thrombospondin-5) is expressed by human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2001, 21:47-54.
56. Risher W.C., Eroglu C. Thrombospondins as key regulators of synaptogenesis in the central nervous system. Matrix Biol. 2012, 31:170-177.
57. Roberts D.D., Miller T.W., Rogers N.M., Yao M., Isenberg J.S. The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47. Matrix Biol. 2012, 31:162-169.
58. Rosenberg R.D., de Agostini A.I. New approaches for defining sequence specific synthesis of heparan sulfate chains. Adv. Exp. Med. Biol. 1992, 313:307-316.
59. Rumsey S.C., Obunike J.C., Arad Y., Deckelbaum R.J., Goldberg I.J. Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibroblasts and macrophages. J. Clin. Invest. 1992, 90:1504-1512.
60. Shimada K., Gill P.J., Silbert J.E., Douglas W.H., Fanburg B.L. Involvement of cell surface heparin sulfate in the binding of lipoprotein lipase to cultured bovine endothelial cells. J. Clin. Invest. 1981, 68:995-1002.
61. Smith J.P., Hicks P.S., Ortiz L.R., Martinez M.J., Mandler R.N. Quantitative measurement of muscle strength in the mouse. J. Neurosci. Methods 1995, 62:15-19.
62. Sodersten F., Ekman S., Schmitz M., Paulsson M., Zaucke F. Thrombospondin-4 and cartilage oligomeric matrix protein form heterooligomers in equine tendon. Connect. Tissue Res. 2006, 47:85-91.
63. Stenina O.I., Desai S.Y., Krukovets I., Kight K., Janigro D., Topol E.J., Plow E.F. Thrombospondin-4 and its variants: expression and differential effects on endothelial cells. Circulation 2003, 108:1514-1519.
64. Stenina O.I., Byzova T.V., Adams J.C., McCarthy J.J., Topol E.J., Plow E.F. Coronary artery disease and the thrombospondin single nucleotide polymorphisms. Int. J. Biochem. Cell Biol. 2004, 36:1013-1030.
65. Stenina O.I., Topol E.J., Plow E.F. Thrombospondins, their polymorphisms, and cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1886-1894.
66. Svensson L., Aszodi A., Heinegard D., Hunziker E.B., Reinholt F.P., Fassler R., Oldberg A. Cartilage oligomeric matrix protein-deficient mice have normal skeletal development. Mol. Cell. Biol. 2002, 22:4366-4371.
67. Sweetwyne M.T., Murphy-Ullrich J.E. Thrombospondin1 in tissue repair and fibrosis: TGF-beta-dependent and independent mechanisms. Matrix Biol. 2012, 31:178-186.
68. Topol E.J., McCarthy J., Gabriel S., Moliterno D.J., Rogers W.J., Newby L.K., Freedman M., Metivier J., Cannata R., O'Donnell C.J., Kottke-Marchant K., Murugesan G., Plow E.F., Stenina O., Daley G.Q. Single nucleotide polymorphisms in multiple novel thrombospondin genes may be associated with familial premature myocardial infarction. Circulation 2001, 104:2641-2644.
69. van Kuppevelt T.H., Dennissen M.A., van Venrooij W.J., Hoet R.M., Veerkamp J.H. Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology. Further evidence for heparan sulfate heterogeneity in the kidney. J. Biol. Chem. 1998, 273:12960-12966.
70. van Kuppevelt T.H., Jenniskens G.J., Veerkamp J.H., ten Dam G.B., Dennissen M.A. Phage display technology to obtain antiheparan sulfate antibodies. Methods Mol. Biol. 2001, 171:519-534.
71. Walton B., W.J., Coresh J., Boerwinkle E. Thrombospondin-2 and Lymphotoxin-a gene variations predict coronary heart disease in a large prospective study. Circulation 2003, 108:IV-771. (Suppl.).
72. Wessel J., Topol E.J., Ji M., Meyer J., McCarthy J.J. Replication of the association between the thrombospondin-4 A387P polymorphism and myocardial infarction. Am. Heart J. 2004, 147:905-909.
73. Williams K.J., Fless G.M., Petrie K.A., Snyder M.L., Brocia R.W., Swenson T.L. Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins. Roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J. Biol. Chem. 1992, 267:13284-13292.
74. Yamada Y., Izawa H., Ichihara S., Takatsu F., Ishihara H., Hirayama H., Sone T., Tanaka M., Yokota M. Prediction of the risk of myocardial infarction from polymorphisms in candidate genes. N. Engl. J. Med. 2002, 347:1916-1923.
75. Ye S., Luo Y., Lu W., Jones R.B., Linhardt R.J., Capila I., Toida T., Kan M., Pelletier H., McKeehan W.L. Structural basis for interaction of FGF-1, FGF-2, and FGF-7 with different heparan sulfate motifs. Biochemistry 2001, 40:14429-14439.
76. Zhang G., Ezura Y., Chervoneva I., Robinson P.S., Beason D.P., Carine E.T., Soslowsky L.J., Iozzo R.V., Birk D.E. Decorin regulates assembly of collagen fibrils and acquisition of biomechanical properties during tendon development. J. Cell. Biochem. 2006, 98:1436-1449.