Degradomic and yeast 2-hybrid inactive catalytic domain substrate trapping identifies new membrane-type 1 matrix metalloproteinase (MMP14) substrates: CCN3 (Nov) and CCN5 (WISP2)

Matrix Biology

Volumn 59, Issue , 2017, Pages 23-38

  Butler, Georgina S ^a   Connor, Andrea R ^a   Sounni, Nor Eddine ^a   Eckhard, Ulrich ^a   Morrison, Charlotte J ^a   Noël, Agnès ^a   Overall, Christopher M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

CCN; Degradomics; ICAT; Inactive catalytic domain capture; MMP; Proteolysis; Substrate trap; Yeast two hybrid

Indexed keywords

ANGIOGENESIS INHIBITOR; BATIMASTAT; CCN5 PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; CYSTEINE RICH PROTEIN 61; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRILYSIN; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; NEUTROPHIL COLLAGENASE; STROMELYSIN; UNCLASSIFIED DRUG; VIMENTIN; CCN PROTEIN; MMP14 PROTEIN, HUMAN; NOV PROTEIN, HUMAN; PROTEIN BINDING; RECOMBINANT PROTEIN; REPRESSOR PROTEIN; WISP2 PROTEIN, HUMAN;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULAR CLONING; PRIORITY JOURNAL; SEQUENCE ANALYSIS; WESTERN BLOTTING; YEAST; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE VECTOR; GENETICS; MCF-7 CELL LINE; METABOLISM; MOLECULAR MODEL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; BINDING SITES; CCN INTERCELLULAR SIGNALING PROTEINS; CLONING, MOLECULAR; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC VECTORS; HELA CELLS; HUMANS; MATRIX METALLOPROTEINASE 14; MCF-7 CELLS; MODELS, MOLECULAR; NEPHROBLASTOMA OVEREXPRESSED PROTEIN; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEOLYSIS; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84994739589     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2016.07.006     Document Type: Article

References (101)

1. [1] Butler, G.S., Overall, C.M., Updated biological roles for matrix metalloproteinases and new “intracellular” substrates revealed by degradomics. Biochemistry 48 (2009), 10830–10845.
2. [2] Cauwe, B., Steen, P.E., Opdenakker, G., The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit. Rev. Biochem. Mol. Biol. 42 (2007), 113–185.
3. [3] Wells, J.M., Gaggar, A., Blalock, J.E., MMP generated matrikines. Matrix Biol. 44–46 (2015), 122–129.
4. [4] McQuibban, G.A., Gong, J.H., Tam, E.M., McCulloch, C.A., Clark-Lewis, I., Overall, C.M., Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289 (2000), 1202–1206.
5. [5] Su, G., Blaine, S.A., Qiao, D., Friedl, A., Membrane type 1 matrix metalloproteinase-mediated stromal syndecan-1 shedding stimulates breast carcinoma cell proliferation. Cancer Res. 68 (2008), 9558–9565.
6. [6] Sounni, N.E., Noel, A., Membrane type-matrix metalloproteinases and tumor progression. Biochimie 87 (2005), 329–342.
7. [7] Genis, L., Galvez, B.G., Gonzalo, P., Arroyo, A.G., MT1-MMP: universal or particular player in angiogenesis?. Cancer Metastasis Rev. 25 (2006), 77–86.
8. [8] Itoh, Y., MT1-MMP: a key regulator of cell migration in tissue. IUBMB Life 58 (2006), 589–596.
9. [9] Hiraoka, N., Allen, E., Apel, I.J., Gyetko, M.R., Weiss, S.J., Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95 (1998), 365–377.
10. [10] Kajita, M., Itoh, Y., Chiba, T., Mori, H., Okada, A., Kinoh, H., Seiki, M., Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153 (2001), 893–904.
11. [11] Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, T., Furukawa, M., Sato, H., Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278 (2003), 40764–40770.
12. [12] Deryugina, E.I., Ratnikov, B.I., Postnova, T.I., Rozanov, D.V., Strongin, A.Y., Processing of integrin alpha(v) subunit by membrane type 1 matrix metalloproteinase stimulates migration of breast carcinoma cells on vitronectin and enhances tyrosine phosphorylation of focal adhesion kinase. J. Biol. Chem. 277 (2002), 9749–9756.
13. [13] Koshikawa, N., Giannelli, G., Cirulli, V., Miyazaki, K., Quaranta, V., Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J. Cell Biol. 148 (2000), 615–624.
14. [14] Sounni, N.E., Roghi, C., Chabottaux, V., Janssen, M., Munaut, C., Maquoi, E., Galvez, B.G., Gilles, C., Frankenne, F., Murphy, G., et al. Up-regulation of vascular endothelial growth factor-A by active membrane-type 1 matrix metalloproteinase through activation of Src-tyrosine kinases. J. Biol. Chem. 279 (2004), 13564–13574.
15. [15] Sounni, N.E., Devy, L., Hajitou, A., Frankenne, F., Munaut, C., Gilles, C., Deroanne, C., Thompson, E.W., Foidart, J.M., Noel, A., MT1-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression. FASEB J. 16 (2002), 555–564.
16. [16] Deryugina, E.I., Soroceanu, L., Strongin, A.Y., Up-regulation of vascular endothelial growth factor by membrane-type 1 matrix metalloproteinase stimulates human glioma xenograft growth and angiogenesis. Cancer Res. 62 (2002), 580–588.
17. [17] Basile, J.R., Holmbeck, K., Bugge, T.H., Gutkind, J.S., MT1-MMP controls tumor-induced angiogenesis through the release of semaphorin 4D. J. Biol. Chem. 282 (2007), 6899–6905.
18. [18] Mu, D., Cambier, S., Fjellbirkeland, L., Baron, J.L., Munger, J.S., Kawakatsu, H., Sheppard, D., Broaddus, V.C., Nishimura, S.L., The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 157 (2002), 493–507.
19. [19] Alfranca, A., Lopez-Oliva, J.M., Genis, L., Lopez-Maderuelo, D., Mirones, I., Salvado, D., Quesada, A.J., Arroyo, A.G., Redondo, J.M., PGE2 induces angiogenesis via MT1-MMP-mediated activation of the TGFbeta/Alk5 signaling pathway. Blood 112 (2008), 1120–1128.
20. [20] Velasco-Loyden, G., Arribas, J., Lopez-Casillas, F., The shedding of betaglycan is regulated by pervanadate and mediated by membrane type matrix metalloprotease-1. J. Biol. Chem. 279 (2004), 7721–7733.
21. [21] Mimura, T., Han, K.Y., Onguchi, T., Chang, J.H., Kim, T.I., Kojima, T., Zhou, Z., Azar, D.T., MT1-MMP-mediated cleavage of decorin in corneal angiogenesis. J. Vasc. Res. 46 (2009), 541–550.
22. [22] Sato, H., Takino, T., Kinoshita, T., Imai, K., Okada, Y., Stetler Stevenson, W.G., Seiki, M., Cell surface binding and activation of gelatinase A induced by expression of membrane-type-1-matrix metalloproteinase (MT1-MMP). FEBS Lett. 385 (1996), 238–240.
23. [23] Will, H., Atkinson, S.J., Butler, G.S., Smith, B., Murphy, G., The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation. Regulation by TIMP-2 and TIMP-3. J. Biol. Chem. 271 (1996), 17119–17123.
24. [24] Knauper, V., Will, H., Lopez-Otin, C., Smith, B., Atkinson, S.J., Stanton, H., Hembry, R.M., Murphy, G., Cellular mechanisms for human procollagenase-3 (MMP-13) activation. Evidence that MT1-MMP (MMP-14) and gelatinase a (MMP-2) are able to generate active enzyme. J. Biol. Chem. 271 (1996), 17124–17131.
25. [25] Maple, J., Moller, S.G., Yeast two-hybrid screening. Methods Mol. Biol. 362 (2007), 207–223.
26. [26] Young, K.H., Yeast two-hybrid: so many interactions, (in) so little time. Biol. Reprod. 58 (1998), 302–311.
27. [27] Tomasetto, C., Masson, R., Linares, J.L., Wendling, C., Lefebvre, O., Chenard, M.P., Rio, M.C., pS2/TFF1 interacts directly with the VWFC cysteine-rich domains of mucins. Gastroenterology 118 (2000), 70–80.
28. [28] Overall, C.M., Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22 (2002), 51–86.
29. [29] Lopez-Otin, C., Overall, C.M., Protease degradomics: a new challenge for proteomics. Nat. Rev. Mol. Cell Biol. 3 (2002), 509–519.
30. [30] Holbourn, K.P., Perbal, B., Ravi Acharya, K., Proteins on the catwalk: modelling the structural domains of the CCN family of proteins. J. Cell. Commun Signal. 3 (2009), 25–41.
31. [31] Holbourn, K.P., Acharya, K.R., Perbal, B., The CCN family of proteins: structure-function relationships. Trends Biochem. Sci. 33 (2008), 461–473.
32. [32] Krupska, I., Bruford, E.A., Chaqour, B., Eyeing the Cyr61/CTGF/NOV (CCN) group of genes in development and diseases: highlights of their structural likenesses and functional dissimilarities. Hum. Genomics, 9, 2015, 24.
33. [33] Mercurio, S., Latinkic, B., Itasaki, N., Krumlauf, R., Smith, J.C., Connective-tissue growth factor modulates WNT signalling and interacts with the WNT receptor complex. Development 131 (2004), 2137–2147.
34. [34] Fu, C.T., Bechberger, J.F., Ozog, M.A., Perbal, B., Naus, C.C., CCN3 (NOV) interacts with connexin43 in C6 glioma cells: possible mechanism of connexin-mediated growth suppression. J. Biol. Chem. 279 (2004), 36943–36950.
35. [35] Gellhaus, A., Dong, X., Propson, S., Maass, K., Klein-Hitpass, L., Kibschull, M., Traub, O., Willecke, K., Perbal, B., Lye, S.J., et al. Connexin43 interacts with NOV: a possible mechanism for negative regulation of cell growth in choriocarcinoma cells. J. Biol. Chem. 279 (2004), 36931–36942.
36. [36] Sakamoto, K., Yamaguchi, S., Ando, R., Miyawaki, A., Kabasawa, Y., Takagi, M., Li, C.L., Perbal, B., Katsube, K., The nephroblastoma overexpressed gene (NOV/ccn3) protein associates with Notch1 extracellular domain and inhibits myoblast differentiation via Notch signaling pathway. J. Biol. Chem. 277 (2002), 29399–29405.
37. [37] Inoki, I., Shiomi, T., Hashimoto, G., Enomoto, H., Nakamura, H., Makino, K., Ikeda, E., Takata, S., Kobayashi, K., Okada, Y., Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J. 16 (2002), 219–221.
38. [38] Perbal, B., Martinerie, C., Sainson, R., Werner, M., He, B., Roizman, B., The C-terminal domain of the regulatory protein NOVH is sufficient to promote interaction with fibulin 1C: a clue for a role of NOVH in cell-adhesion signaling. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 869–874.
39. [39] Grzeszkiewicz, T.M., Kirschling, D.J., Chen, N., Lau, L.F., CYR61 stimulates human skin fibroblast migration through integrin alpha vbeta 5 and enhances mitogenesis through integrin alpha vbeta 3, independent of its carboxyl-terminal domain. J. Biol. Chem. 276 (2001), 21943–21950.
40. [40] Chen, N., Chen, C.C., Lau, L.F., Adhesion of human skin fibroblasts to Cyr61 is mediated through integrin alpha 6beta 1 and cell surface heparan sulfate proteoglycans. J. Biol. Chem. 275 (2000), 24953–24961.
41. [41] Jun, J.I., Lau, L.F., Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat. Rev. Drug Discov. 10 (2011), 945–963.
42. [42] Leask, A., Abraham, D.J., All in the CCN family: essential matricellular signaling modulators emerge from the bunker. J. Cell Sci. 119 (2006), 4803–4810.
43. [43] Lau, L.F., Lam, S.C., The CCN family of angiogenic regulators: the integrin connection. Exp. Cell Res. 248 (1999), 44–57.
44. [44] Wahab, N.A., Brinkman, H., Mason, R.M., Uptake and intracellular transport of the connective tissue growth factor: a potential mode of action. Biochem. J. 359 (2001), 89–97.
45. [45] Tamura, I., Rosenbloom, J., Macarak, E., Chaqour, B., Regulation of Cyr61 gene expression by mechanical stretch through multiple signaling pathways. Am. J. Phys. Cell Physiol. 281 (2001), C1524–C1532.
46. [46] Perbal, B., Nuclear localisation of NOVH protein: a potential role for NOV in the regulation of gene expression. Mol. Pathol. 52 (1999), 84–91.
47. [47] Planque, N., Long Li, C., Saule, S., Bleau, A.M., Perbal, B., Nuclear addressing provides a clue for the transforming activity of amino-truncated CCN3 proteins. J. Cell. Biochem. 99 (2006), 105–116.
48. [48] Wiesman, K.C., Wei, L., Baughman, C., Russo, J., Gray, M.R., Castellot, J.J., CCN5, a secreted protein, localizes to the nucleus. J. Cell. Commun Signal. 4 (2010), 91–98.
49. [49] Sabbah, M., Prunier, C., Ferrand, N., Megalophonos, V., Lambein, K., De Wever, O., Nazaret, N., Lachuer, J., Dumont, S., Redeuilh, G., CCN5, a novel transcriptional repressor of the transforming growth factor beta signaling pathway. Mol. Cell. Biol. 31 (2011), 1459–1469.
50. [50] Yang, D.H., Kim, H.S., Wilson, E.M., Rosenfeld, R.G., Oh, Y., Identification of glycosylated 38-kDa connective tissue growth factor (IGFBP-related protein 2) and proteolytic fragments in human biological fluids, and up-regulation of IGFBP-rP2 expression by TGF-beta in Hs578T human breast cancer cells. J. Clin. Endocrinol. Metab. 83 (1998), 2593–2596.
51. [51] Roestenberg, P., van Nieuwenhoven, F.A., Wieten, L., Boer, P., Diekman, T., Tiller, A.M., Wiersinga, W.M., Oliver, N., Usinger, W., Weitz, S., et al. Connective tissue growth factor is increased in plasma of type 1 diabetic patients with nephropathy. Diabetes Care 27 (2004), 1164–1170.
52. [52] Burren, C.P., Wilson, E.M., Hwa, V., Oh, Y., Rosenfeld, R.G., Binding properties and distribution of insulin-like growth factor binding protein-related protein 3 (IGFBP-rP3/NovH), an additional member of the IGFBP superfamily. J. Clin. Endocrinol. Metab. 84 (1999), 1096–1103.
53. [53] Su, B.Y., Cai, W.Q., Zhang, C.G., Martinez, V., Lombet, A., Perbal, B., The expression of ccn3 (nov) RNA and protein in the rat central nervous system is developmentally regulated. Mol. Pathol. 54 (2001), 184–191.
54. [54] Schlage, P., U., a.d.K., Proteomic approaches to uncover MMP function. Matrix Biol. 44-46 (2015), 232–238.
55. [55] Kleifeld, O., Doucet, A., U., a.d.K., Prudova, A., Schilling, O., Kainthan, R.K., Starr, A.E., Foster, L.J., Kizhakkedathu, J.N., Overall, C.M., Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat. Biotechnol. 28 (2010), 281–288.
56. [56] Eckhard, U., Marino, G., Abbey, S.R., Tharmarajah, G., Matthew, I., Overall, C.M., The human dental pulp proteome and N-Terminome: levering the unexplored potential of semitryptic peptides enriched by TAILS to identify missing proteins in the human proteome project in underexplored tissues. J. Proteome Res. 14 (2015), 3568–3582.
57. [57] Overall, C.M., Blobel, C.P., In search of partners: linking extracellular proteases to substrates. Nat. Rev. Mol. Cell Biol. 8 (2007), 245–257.
58. [58] Butler, G.S., Dean, R.A., Tam, E.M., Overall, C.M., Pharmacoproteomics of a metalloproteinase hydroxamate inhibitor in breast cancer cells: dynamics of membrane type 1 matrix metalloproteinase-mediated membrane protein shedding. Mol. Cell. Biol. 28 (2008), 4896–4914.
59. [59] Cauwe, B., Martens, E., Proost, P., Opdenakker, G., Multidimensional degradomics identifies systemic autoantigens and intracellular matrix proteins as novel gelatinase B/MMP-9 substrates. Integr. Biol. 1 (2009), 404–426 Camb.
60. [60] Starr, A.E., Bellac, C.L., Dufour, A., Goebeler, V., Overall, C.M., Biochemical characterization and N-terminomics analysis of leukolysin, the membrane-type 6 matrix metalloprotease (MMP25): chemokine and vimentin cleavages enhance cell migration and macrophage phagocytic activities. J. Biol. Chem. 287 (2012), 13382–13395.
61. [61] Masson, V.V., Devy, L., Grignet-Debrus, C., Bernt, S., Bajou, K., Blacher, S., Roland, G., Chang, Y., Fong, T., Carmeliet, P., et al. Mouse aortic ring assay: a new approach of the molecular genetics of angiogenesis. Biol. Proced. Online 4 (2002), 24–31.
62. [62] Tam, E.M., Morrison, C.J., Wu, Y.I., Stack, M.S., Overall, C.M., Membrane protease proteomics: isotope-coded affinity tag MS identification of undescribed MT1-matrix metalloproteinase substrates. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 6917–6922.
63. [63] Dean, R.A., Butler, G.S., Hamma-Kourbali, Y., Delbe, J., Brigstock, D.R., Courty, J., Overall, C.M., Identification of candidate angiogenic inhibitors processed by matrix metalloproteinase 2 (MMP-2) in cell-based proteomic screens: disruption of vascular endothelial growth factor (VEGF)/heparin affin regulatory peptide (pleiotrophin) and VEGF/connective tissue growth factor angiogenic inhibitory complexes by MMP-2 proteolysis. Mol. Cell. Biol. 27 (2007), 8454–8465.
64. [64] Hashimoto, G., Inoki, I., Fujii, Y., Aoki, T., Ikeda, E., Okada, Y., Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165. J. Biol. Chem. 277 (2002), 36288–36295.
65. [65] Choi, J., Lin, A., Shrier, E., Lau, L.F., Grant, M.B., Chaqour, B., Degradome products of the matricellular protein CCN1 as modulators of pathological angiogenesis in the retina. J. Biol. Chem. 288 (2013), 23075–23089.
66. [66] Russo, J.W., Castellot, J.J., CCN5: biology and pathophysiology. J. Cell. Commun Signal. 4 (2010), 119–130.
67. [67] Zhang, R., Averboukh, L., Zhu, W., Zhang, H., Jo, H., Dempsey, P.J., Coffey, R.J., Pardee, A.B., Liang, P., Identification of rCop-1, a new member of the CCN protein family, as a negative regulator for cell transformation. Mol. Cell. Biol. 18 (1998), 6131–6141.
68. [68] Ball, D.K., Moussad, E.E., Rageh, M.A., Kemper, S.A., Brigstock, D.R., Establishment of a recombinant expression system for connective tissue growth factor (CTGF) that models CTGF processing in utero. Reproduction 125 (2003), 271–284.
69. [69] Robinson, P.M., Smith, T.S., Patel, D., Dave, M., Lewin, A.S., Pi, L., Scott, E.W., Tuli, S.S., Schultz, G.S., Proteolytic processing of connective tissue growth factor in normal ocular tissues and during corneal wound healing. Invest. Ophthalmol. Vis. Sci. 53 (2012), 8093–8103.
70. [70] Guillon-Munos, A., Oikonomopoulou, K., Michel, N., Smith, C.R., Petit-Courty, A., Canepa, S., Reverdiau, P., Heuze-Vourc'h, N., Diamandis, E.P., Courty, Y., Kallikrein-related peptidase 12 hydrolyzes matricellular proteins of the CCN family and modifies interactions of CCN1 and CCN5 with growth factors. J. Biol. Chem. 286 (2012), 25505–25518.
71. [71] Jefferson, T., Auf dem Keller, U., Bellac, C., Metz, V.V., Broder, C., Hedrich, J., Ohler, A., Maier, W., Magdolen, V., Sterchi, E., et al. The substrate degradome of meprin metalloproteases reveals an unexpected proteolytic link between meprin beta and ADAM10. Cell. Mol. Life Sci. 70 (2013), 309–333.
72. [72] Perbal, B., Alternative splicing of CCN mRNAs … it has been upon us. J. Cell. Commun Signal. 3 (2009), 153–157.
73. [73] Murphy-Ullrich, J.E., Sage, E.H., Revisiting the matricellular concept. Matrix Biol. 37 (2014), 1–14.
74. [74] Molla, A., Tanase, S., Hong, Y.M., Maeda, H., Interdomain cleavage of plasma fibronectin by zinc-metalloproteinase from Serratia marcescens. Biochim. Biophys. Acta 955 (1988), 77–85.
75. [75] Doucet, A., Butler, G.S., Rodriguez, D., Prudova, A., Overall, C.M., Metadegradomics: toward in vivo quantitative degradomics of proteolytic post-translational modifications of the cancer proteome. Mol. Cell. Proteomics 7 (2008), 1925–1951.
76. [76] Pendurthi, U.R., Tran, T.T., Post, M., Rao, L.V., Proteolysis of CCN1 by plasmin: functional implications. Cancer Res. 65 (2005), 9705–9711.
77. [77] Brigstock, D.R., Steffen, C.L., Kim, G.Y., Vegunta, R.K., Diehl, J.R., Harding, P.A., Purification and characterization of novel heparin-binding growth factors in uterine secretory fluids. Identification as heparin-regulated Mr 10,000 forms of connective tissue growth factor. J. Biol. Chem. 272 (1997), 20275–20282.
78. [78] Steffen, C.L., Ball-Mirth, D.K., Harding, P.A., Bhattacharyya, N., Pillai, S., Brigstock, D.R., Characterization of cell-associated and soluble forms of connective tissue growth factor (CTGF) produced by fibroblast cells in vitro. Growth Factors 15 (1998), 199–213.
79. [79] Ball, D.K., Rachfal, A.W., Kemper, S.A., Brigstock, D.R., The heparin-binding 10 kDa fragment of connective tissue growth factor (CTGF) containing module 4 alone stimulates cell adhesion. J. Endocrinol. 176 (2003), R1–R7.
80. [80] Gao, R., Brigstock, D.R., A novel integrin alpha5beta1 binding domain in module 4 of connective tissue growth factor (CCN2/CTGF) promotes adhesion and migration of activated pancreatic stellate cells. Gut 55 (2006), 856–862.
81. [81] Aoyama, E., Hattori, T., Hoshijima, M., Araki, D., Nishida, T., Kubota, S., Takigawa, M., N-terminal domains of CCN family 2/connective tissue growth factor bind to aggrecan. Biochem. J. 420 (2009), 413–420.
82. [82] Tong, Z.Y., Brigstock, D.R., Intrinsic biological activity of the thrombospondin structural homology repeat in connective tissue growth factor. J. Endocrinol. 188 (2006), R1–R8.
83. [83] Joliot, V., Martinerie, C., Dambrine, G., Plassiart, G., Brisac, M., Crochet, J., Perbal, B., Proviral rearrangements and overexpression of a new cellular gene (nov) in myeloblastosis-associated virus type 1-induced nephroblastomas. Mol. Cell. Biol. 12 (1992), 10–21.
84. [84] Laurent, M., Martinerie, C., Thibout, H., Hoffman, M.P., Verrecchia, F., Le Bouc, Y., Mauviel, A., Kleinman, H.K., NOVH increases MMP3 expression and cell migration in glioblastoma cells via a PDGFR-alpha-dependent mechanism. FASEB J. 17 (2003), 1919–1921.
85. [85] Bleau, A.M., Planque, N., Lazar, N., Zambelli, D., Ori, A., Quan, T., Fisher, G., Scotlandi, K., Perbal, B., Antiproliferative activity of CCN3: involvement of the C-terminal module and post-translational regulation. J. Cell. Biochem. 101 (2007), 1475–1491.
86. [86] Mandal, S.K., Rao, L.V., Tran, T.T., Pendurthi, U.R., A novel mechanism of plasmin-induced mitogenesis in fibroblasts. J. Thromb. Haemost. 3 (2005), 163–169.
87. [87] Lafont, J., Thibout, H., Dubois, C., Laurent, M., Martinerie, C., NOV/CCN3 induces adhesion of muscle skeletal cells and cooperates with FGF2 and IGF-1 to promote proliferation and survival. Cell Commun. Adhes. 12 (2005), 41–57.
88. [88] Kubota, S., Takigawa, M., CCN family proteins and angiogenesis: from embryo to adulthood. Angiogenesis 10 (2007), 1–11.
89. [89] Karagiannis, E.D., Popel, A.S., Peptides derived from type I thrombospondin repeat-containing proteins of the CCN family inhibit proliferation and migration of endothelial cells. Int. J. Biochem. Cell Biol. 39 (2007), 2314–2323.
90. [90] Notari, L., Miller, A., Martinez, A., Amaral, J., Ju, M., Robinson, G., Smith, L.E., Becerra, S.P., Pigment epithelium-derived factor is a substrate for matrix metalloproteinase type 2 and type 9: implications for downregulation in hypoxia. Invest. Ophthalmol. Vis. Sci. 46 (2005), 2736–2747.
91. [91] Yoon, P.O., Lee, M.A., Cha, H., Jeong, M.H., Kim, J., Jang, S.P., Choi, B.Y., Jeong, D., Yang, D.K., Hajjar, R.J., et al. The opposing effects of CCN2 and CCN5 on the development of cardiac hypertrophy and fibrosis. J. Mol. Cell. Cardiol. 49 (2010), 294–303.
92. [92] Tan, T.W., Yang, W.H., Lin, Y.T., Hsu, S.F., Li, T.M., Kao, S.T., Chen, W.C., Fong, Y.C., Tang, C.H., Cyr61 increases migration and MMP-13 expression via alphavbeta3 integrin, FAK, ERK and AP-1-dependent pathway in human chondrosarcoma cells. Carcinogenesis 30 (2009), 258–268.
93. [93] Banerjee, S., Dhar, G., Haque, I., Kambhampati, S., Mehta, S., Sengupta, K., Tawfik, O., Phillips, T.A., Banerjee, S.K., CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Cancer Res. 68 (2008), 7606–7612.
94. [94] Lake, A.C., Castellot, J.J. Jr., CCN5 modulates the antiproliferative effect of heparin and regulates cell motility in vascular smooth muscle cells. Cell. Commun. Signal, 1, 2003, 5.
95. [95] Fields, S., Song, O., A novel genetic system to detect protein-protein interactions. Nature 340 (1989), 245–246.
96. [96] Butler, G.S., Dean, R.A., Smith, D., Overall, C.M., Membrane protease degradomics: proteomic identification and quantification of cell surface protease substrates. Methods Mol. Biol. 528 (2009), 159–176.
97. [97] Wallon, U.M., Overall, C.M., The hemopexin-like domain (C domain) of human gelatinase A (matrix metalloproteinase-2) requires Ca2 + for fibronectin and heparin binding. Binding properties of recombinant gelatinase A C domain to extracellular matrix and basement membrane components. J. Biol. Chem. 272 (1997), 7473–7481.
98. [98] Clark-Lewis, I., Hood, L.E., Kent, S.B., Role of disulfide bridges in determining the biological activity of interleukin 3. Proc. Natl. Acad. Sci. U. S. A. 85 (1988), 7897–7901.
99. [99] Morrison, C.J., Butler, G.S., Bigg, H.F., Roberts, C.R., Soloway, P.D., Overall, C.M., Cellular activation of MMP-2 (gelatinase A) by MT2-MMP occurs via a TIMP-2-independent pathway. J. Biol. Chem. 276 (2001), 47402–47410.
100. [100] Blacher, S., Devy, L., Burbridge, M.F., Roland, G., Tucker, G., Noel, A., Foidart, J.M., Improved quantification of angiogenesis in the rat aortic ring assay. Angiogenesis 4 (2001), 133–142.
101. [101] Zhang, Y., I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 40, 2008, 10.1186/1471-2105-9-40.