A current view of perlecan in physiology and pathology: A mosaic of functions

Matrix Biology

Volumn 57-58, Issue , 2017, Pages 285-298

  Gubbiotti, Maria A ^a   Neill, Thomas ^a   Iozzo, Renato V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Angiogenesis; Autophagy; Endorepellin; Heparan sulfate; Proteoglycan

Indexed keywords

ADENOSINE PHOSPHATE; IMMUNOGLOBULIN; LAMININ; LAMININ A; MAMMALIAN TARGET OF RAPAMYCIN; NERVE CELL ADHESION MOLECULE; PERLECAN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; ENDOREPELLIN PROTEIN, HUMAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; KDR PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; PEPTIDE FRAGMENT; PROTEOHEPARAN SULFATE; TARGET OF RAPAMYCIN KINASE;

AMINO TERMINAL SEQUENCE; ANGIOGENESIS; ATHEROSCLEROSIS; AUTOPHAGY; BIOLOGICAL FUNCTIONS; CARBOXY TERMINAL SEQUENCE; EXTRACELLULAR MATRIX; GENE STRUCTURE; GENETIC REGULATION; GENOMICS; HUMAN; MOSAICISM; NONHUMAN; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; BASEMENT MEMBRANE; BONE DEVELOPMENT; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; INFLAMMATION; METABOLISM; ORGANOGENESIS; PROTEIN DOMAIN;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; BASEMENT MEMBRANE; GENE EXPRESSION REGULATION; HEART; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; INFLAMMATION; NEOVASCULARIZATION, PHYSIOLOGIC; ORGANOGENESIS; OSTEOGENESIS; PEPTIDE FRAGMENTS; PROTEIN DOMAINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84992695428     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2016.09.003     Document Type: Review

References (160)

1. [1] Iozzo, R.V., Schaefer, L., Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol. 42 (2015), 11–55.
2. [2] Iozzo, R.V., Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67 (1998), 609–652.
3. [3] Naba, A., Clauser, K.R., Ding, H., Whittaker, C.A., Carr, S.A., Hynes, R.O., The extracellular matrix: tools and insights for the “omics” era. Matrix Biol. 49 (2016), 10–24.
4. [4] Hassell, J.R., Leyshon, W.C., Ledbetter, S.R., Tyree, B., Suzuki, S., Kato, M., et al. Isolation of two forms of basement membrane proteoglycans. J. Biol. Chem. 260 (1985), 8098–8105.
5. [5] Iozzo, R.V., Hassell, J.R., Identification of the precursor protein for the heparan sulfate proteoglycan of human colon carcinoma cells and its post-translational modifications. Arch. Biochem. Biophys. 269 (1989), 239–249.
6. [6] Iozzo, R.V., Biosynthesis of heparan sulfate proteoglycan by human colon carcinoma cells and its localization at the cell surface. J. Cell Biol. 99 (1984), 403–417.
7. [7] Yurchenco, P.D., Cheng, Y.-S., Ruben, G.C., Self-assembly of a high molecular weight basement membrane heparan sulfate proteoglycan into dimers and oligomers. J. Biol. Chem. 262 (1987), 17668–17676.
8. [8] Murdoch, A.D., Liu, B., Schwarting, R., Tuan, R.S., Iozzo, R.V., Widespread expression of perlecan proteoglycan in basement membranes and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization. J. Histochem. Cytochem. 42 (1994), 239–249.
9. [9] McCarthy, K.J., The basement membrane proteoglycans perlecan and agrin: something old, something new. Curr. Top. Membr. 76 (2015), 255–303.
10. [10] Whitelock, J.M., Graham, L.D., Melrose, J., Murdoch, A.D., Iozzo, R.V., Underwood, P.A., Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol. 18 (1999), 163–178.
11. [11] Lord, M.S., Chuang, C.Y., Melrose, J., Davies, M.J., Iozzo, R.V., Whitelock, J.M., The role of vascular-derived perlecan in modulating cell adhesion, proliferation and growth factor signaling. Matrix Biol. 35 (2014), 112–122.
12. [12] Christianson, H.C., Belting, M., Heparan sulfate proteoglycan as a cell-surface endocytosis receptor. Matrix Biol. 35 (2014), 51–55.
13. [13] Hassell, J.R., Yamada, Y., Arikawa-Hirasawa, E., Role of perlecan in skeletal development and diseases. Glycoconj. J. 19 (2003), 263–267.
14. [14] Jochmann, K., Bachvarova, V., Vortkamp, A., Heparan sulfate as a regulator of endochondral ossification and osteochondroma development. Matrix Biol. 34 (2014), 55–63.
15. [15] Wilusz, R.E., Sanchez-Adams, J., Guilak, F., The structure and function of the pericellular matrix of articular cartilage. Matrix Biol. 39 (2014), 25–32.
16. [16] Hsueh, M.F., Onnerfjord, P., Kraus, V.B., Biomarkers and proteomic analysis of osteoarthritis. Matrix Biol. 39 (2014), 56–66.
17. [17] Fuki, I., Iozzo, R.V., Williams, K.J., Perlecan heparan sulfate proteoglycan. A novel receptor that mediates a distinct pathway for ligand catabolism. J. Biol. Chem. 275 (2000), 25742–25750.
18. [18] Colombelli, C., Palmisano, M., Eshed-Eisenbach, Y., Zambroni, D., Pavoni, E., Ferri, C., et al. Perlecan is recruited by dystroglycan to nodes of Ranvier and binds the clustering molecule gliomedin. J. Cell Biol. 208 (2015), 313–329.
19. [19] Lord, M.S., Jung, M., Cheng, B., Whitelock, J.M., Transcriptional complexity of the HSPG2 gene in the human mast cell line, HMC-1. Matrix Biol. 35 (2014), 123–131.
20. [20] Jung, M., Lord, M.S., Cheng, B., Lyons, J.G., Alkhouri, H., Hughes, J.M., et al. Mast cells produce novel shorter forms of perlecan that contain functional endorepellin: a role in angiogenesis and wound healing. J. Biol. Chem. 288 (2013), 3289–3304.
21. [21] Nugent, M.A., Nugent, H.M., Iozzo, R.V., Sanchack, K., Edelman, E.R., Perlecan is required to inhibit thrombosis after deep vascular injury and contributes to endothelial cell-mediated inhibition of intimal hyperplasia. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 6722–6727.
22. [22] Cohen, I.R., Murdoch, A.D., Naso, M.F., Marchetti, D., Berd, D., Iozzo, R.V., Abnormal expression of perlecan proteoglycan in metastatic melanomas. Cancer Res. 54 (1994), 5771–5774.
23. [23] Iozzo, R.V., Proteoglycans and neoplasia. Cancer Metastasis Rev. 7 (1988), 39–50.
24. [24] Mathiak, M., Yenisey, C., Grant, D.S., Sharma, B., Iozzo, R.V., A role for perlecan in the suppression of growth and invasion in fibrosarcoma cells. Cancer Res. 57 (1997), 2130–2136.
25. [25] Mongiat, M., Sweeney, S., San Antonio, J.D., Fu, J., Iozzo, R.V., Endorepellin, a novel inhibitor of angiogenesis derived from the C terminus of perlecan. J. Biol. Chem. 278 (2003), 4238–4249.
26. [26] Iozzo, R.V., San Antonio, J.D., Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J. Clin. Invest. 108 (2001), 349–355.
27. [27] Iozzo, R.V., Zoeller, J.J., Nyström, A., Basement membrane proteoglycans: modulators par excellence of cancer growth and angiogenesis. Mol. Cell 27 (2009), 503–513.
28. [28] Iozzo, R.V., Sanderson, R.D., Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 15 (2011), 1013–1031.
29. [29] Grindel, B.J., Martinez, J.R., Pennington, C.L., Muldoon, M., Stave, J., Chung, L.W., et al. Matrilysin/matrix metalloproteinase-7(MMP7) cleavage of perlecan/HSPG2 creates a molecular switch to alter prostate cancer cell behavior. Matrix Biol. 36 (2014), 64–76.
30. [30] Qiang, B., Lim, S.Y., Lekas, M., Kuliszewski, M.A., Wolff, R., Osherov, A.B., et al. Perlecan heparan sulfate proteoglycan is a critical determinant of angiogenesis in response to mouse hind-limb ischemia. Can. J. Cardiol. 30 (2014), 1444–1451.
31. [31] Poluzzi, C., Iozzo, R.V., Schaefer, L., Endostatin and endorepellin: a common route of action for similar angiostatic cancer avengers. Adv. Drug Deliv. Rev. 97 (2016), 156–173.
32. [32] Theocharis, A.D., Gialeli, C., Bouris, P., Giannopoulou, E., Skandalis, S.S., Aletras, A.J., et al. Cell-matrix interactions: focus on proteoglycan-proteinase interplay and pharmacological targeting in cancer. FEBS J. 281 (2014), 5023–5042.
33. [33] Theocharis, A.D., Skandalis, S.S., Neill, T., Multhaupt, H.A., Hubo, M., Frey, H., et al. Insights into the key roles of proteoglycans in breast cancer biology and translational medicine. Biochim. Biophys. Acta 1855 (2015), 276–300.
34. [34] Zoeller, J.J., McQuillan, A., Whitelock, J., Ho, S.-Y., Iozzo, R.V., A central function for perlecan in skeletal muscle and cardiovascular development. J. Cell Biol. 181 (2008), 381–394.
35. [35] Poluzzi, C., Casulli, J., Goyal, A., Mercer, T.J., Neill, T., Iozzo, R.V., Endorepellin evokes autophagy in endothelial cells. J. Biol. Chem. 289 (2014), 16114–16128.
36. [36] Ning, L., Xu, Z., Furuya, N., Nonaka, R., Yamada, Y., Arikawa-Hirasawa, E., Perlecan inhibits autophagy to maintain muscle homeostasis in mouse soleus muscle. Matrix Biol. 48 (2015), 26–35.
37. [37] Murdoch, A.D., Dodge, G.R., Cohen, I., Tuan, R.S., Iozzo, R.V., Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Biol. Chem. 267 (1992), 8544–8557.
38. [38] Farach-Carson, M.C., Warren, C.R., Harrington, D.A., Carson, D.D., Border patrol: insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol. 34 (2014), 64–79.
39. [39] Noonan, D.M., Fulle, A., Valente, P., Cai, S., Horigan, E., Sasaki, M., et al. The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin a chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J. Biol. Chem. 266 (1991), 22939–22947.
40. [40] Cohen, I.R., Grässel, S., Murdoch, A.D., Iozzo, R.V., Structural characterization of the complete human perlecan gene and its promoter. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 10404–10408.
41. [41] Warren, C.R., Kassir, E., Spurlin, J., Martinez, J., Putnam, N.H., Farach-Carson, M.C., Evolution of the perlecan/HSPG2 gene and its activation in regenerating Nematostella vectensis. PLoS One, 10, 2015, e0124578.
42. [42] Iozzo, R.V., Pillarisetti, J., Sharma, B., Murdoch, A.D., Danielson, K.G., Uitto, J., et al. Structural and functional characterization of the human perlecan gene promoter. Transcriptional activation by transforming factor-β via a nuclear factor 1-binding element. J. Biol. Chem. 272 (1997), 5219–5228.
43. [43] Sharma, B., Iozzo, R.V., Transcriptional silencing of perlecan gene expression by interferon-γ. J. Biol. Chem. 273 (1998), 4642–4646.
44. [44] Warren, C.R., Grindel, B.J., Francis, L., Carson, D.D., Farach-Carson, M.C., Transcriptional activation by NFkappaB increases perlecan/HSPG2 expression in the desmoplastic prostate tumor microenvironment. J. Cell. Biochem. 115 (2014), 1322–1333.
45. [45] Melrose, J., Smith, S., Whitelock, J., Perlecan immunolocalizes to perichondrial vessels and canals in human fetal cartilaginous primordia in early vascular and matrix remodeling events associated with diarthrodial joint development. J. Histochem. Cytochem. 52 (2004), 1405–1413.
46. [46] Smith, S.M., Whitelock, J.M., Iozzo, R.V., Little, C.B., Melrose, J., Topographical variation in the distribution of versican, aggrecan and perlecan in the foetal human spine reflects their diverse functional roles in spinal development. Histochem. Cell Biol. 132 (2009), 491–503.
47. [47] Handler, M., Yurchenco, P.D., Iozzo, R.V., Developmental expression of perlecan during murine embryogenesis. Dev. Dyn. 210 (1997), 130–145.
48. [48] French, M.M., Smith, S.E., Akanbi, K., Sanford, T., Hecht, J., Farach-Carson, M.C., et al. Expression of the heparan sulfate proteoglycan, perlecan, during mouse embryogenesis and perlecan chondrogenic activity in vitro. J. Cell Biol. 145 (1999), 1103–1115.
49. [49] Farach-Carson, M.C., Carson, D.D., Perlecan - a multifunctional extracellular proteoglycan scaffold. Glycobiology 17 (2007), 897–905.
50. [50] Iozzo, R.V., Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 6 (2005), 646–656.
51. [51] Whitelock, J.M., Melrose, J., Iozzo, R.V., Diverse cell signaling events modulated by perlecan. Biochemistry 47 (2008), 11174–11183.
52. [52] Mongiat, M., Otto, J., Oldershaw, R., Ferrer, F., Sato, J.D., Iozzo, R.V., Fibroblast growth factor-binding protein is a novel partner for perlecan protein core. J. Biol. Chem. 276 (2001), 10263–10271.
53. [53] Mongiat, M., Fu, J., Oldershaw, R., Greenhalgh, R., Gown, A., Iozzo, R.V., Perlecan protein core interacts with extracellular matrix protein 1 (ECM1), a glycoprotein involved in bone formation and angiogenesis. J. Biol. Chem. 278 (2003), 17491–17499.
54. [54] Ghiselli, G., Eichstetter, I., Iozzo, R.V., A role for the perlecan protein core in the activation of the keratinocyte growth factor receptor. Biochem. J. 359 (2001), 153–163.
55. [55] Gonzalez, E.M., Mongiat, M., Slater, S.J., Baffa, R., Iozzo, R.V., A novel interaction between perlecan protein core and progranulin: potential effects on tumor growth. J. Biol. Chem. 278 (2003), 38113–38116.
56. [56] Kerever, A., Mercier, F., Nonaka, R., de Vega, S., Oda, Y., B.Zalc, et al. Perlecan is required for FGF-2 signaling in the neural stem cell niche. Stem Cell Res. 12 (2014), 492–505.
57. [57] Wilusz, R.E., DeFrate, L.E., Guilak, F., A biomechanical role for perlecan in the pericellular matrix of articular cartilage. Matrix Biol. 31 (2012), 320–327.
58. [58] Muller, C., Khabut, A., Dudhia, J., Reinholt, F.P., Aspberg, A., Heinegard, D., et al. Quantitative proteomics at different depths in human articular cartilage reveals unique patterns of protein distribution. Matrix Biol. 40 (2014), 34–45.
59. [59] Sadatsuki, R., Kaneko, H., Kinoshita, M., Futami, I., Nonaka, R., Culley, K.L., et al. Perlecan is required for the chondrogenic differentiation of synovial mesenchymal cells through regulation of Sox9 gene expression. J. Orthop. Res., 2016.
60. [60] Sher, I., Zisman-Rozen, S., Eliahu, L., Whitelock, J.M., Maas-Szabowski, N., Yamada, Y., et al. Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation. J. Biol. Chem. 281 (2006), 5178–5187.
61. [61] Ishijima, M., Suzuki, N., Hozumi, K., Matsunobu, T., Kosaki, K., Kaneko, H., et al. Perlecan modulates VEGF signaling and is essential for vascularization in endochondral bone formation. Matrix Biol. 31 (2012), 234–245.
62. [62] Wang, B., Lai, X., Price, C., Thompson, W.R., Li, W., Quabili, T.R., et al. Perlecan-containing pericellular matrix regulates solute transport and mechanosensing within the osteocyte lacunar-canalicular system. J. Bone Miner. Res. 29 (2014), 878–891.
63. [63] Wijeratne, S.S., Martinez, J.R., Grindel, B.J., Frey, E.W., Li, J., Wnag, K., et al. Single molecule force measurements of perlecan/HSPG2: a key component of the osteocyte pericellular matrix. Matrix Biol. 50 (2016), 27–38.
64. [64] Kaneko, H., Ishijima, M., Futami, I., Tomikawa-Ichikawa, N., Kosaki, K., Sadatsuki, R., et al. Synovial perlecan is required for osteophyte formation in knee osteoarthritis. Matrix Biol. 32 (2013), 178–187.
65. [65] Vikramadithyan, R.K., Kako, Y., Chen, G., Hu, Y., Arikawa-Hirasawa, E., Yamada, Y., et al. Atherosclerosis in perlecan heterozygous mice. J. Lipid Res. 45 (2004), 1806–1812.
66. [66] Tran-Lundmark, K., Tannenberg, P., Rauch, B.H., Ekstrand, J., Tran, P.K., Hedin, U., et al. Perlecan heparan sulfate is required for the inhibition of smooth muscle cell proliferation by all-trans-retinoic acid. J. Cell. Physiol. 230 (2015), 482–487.
67. [67] Xu, Z., Ichikawa, N., Kosaki, K., Yamada, Y., Sasaki, T., Sakai, L.Y., et al. Perlecan deficiency causes muscle hypertrophy, a decrease in myostatin expression, and changes in muscle fiber composition. Matrix Biol. 29 (2010), 461–470.
68. [68] Sharma, B., Handler, M., Eichstetter, I., Whitelock, J., Nugent, M.A., Iozzo, R.V., Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo. J. Clin. Invest. 102 (1998), 1599–1608.
69. [69] Douglass, S., Goyal, A., Iozzo, R.V., The role of perlecan and endorepellin in the control of tumor angiogenesis and endothelial cell autophagy. Connect. Tissue Res. 19 (2015), 1–11.
70. [70] Dos, S.M., Michopoulou, A., Andre-Frei, V., Boulesteix, S., Guicher, C., Dayan, G., et al. Perlecan expression influences the keratin 15-positive cell population fate in the epidermis of aging skin. Aging (Albany NY) 8 (2016), 751–768.
71. [71] Chang, Y.T., Tseng, C.N., Tannenberg, P., Eriksson, L., Yuan, K., de Jesus Perez, V.A., et al. Perlecan heparan sulfate deficiency impairs pulmonary vascular development and attenuates hypoxic pulmonary hypertension. Cardiovasc. Res. 107 (2015), 20–31.
72. [72] Mongiat, M., Taylor, K., Otto, J., Aho, S., Uitto, J., Whitelock, J., et al. The protein core of the proteoglycan perlecan binds specifically to fibroblast growth factor-7. J. Biol. Chem. 275 (2000), 7095–7100.
73. [73] Smith, S.M.L., West, L.A., Govindraj, P., Zhang, X., Ornitz, D.M., Hassell, J.R., Heparan and chondroitin sulfate on growth plate perlecan mediate binding and delivery of FGF-2 to FGF receptors. Matrix Biol. 26 (2007), 175–184.
74. [74] Muthusamy, A., Cooper, C.R., Jr. Gomes, R.R., Soluble perlecan domain I enhances vascular endothelial growth factor-165 activity and receptor phosphorylation in human bone marrow endothelial cells. BMC Biochem., 11, 2010, 43.
75. [75] Noonan, D.M., Hassell, J.R., Perlecan, the large low-density proteoglycan of basement membranes: structure and variant forms. Kidney Int. 43 (1993), 53–60.
76. [76] Xu, Y., Ashline, D., Liu, L., Tassa, C., Shaw, S.Y., Ravid, K., et al. The glycosylation-dependent interaction of perlecan core protein with LDL: implications for atherosclerosis. J. Lipid Res. 56 (2015), 266–276.
77. [77] Tran-Lundmark, K., Tran, P.-K., Paulsson-Berne, G., Fridén, V., Soinen, R., Tryggvason, K., et al. Heparan sulfate in perlecan promotes mouse atherosclerosis. Roles of lipid permeability, lipid retention, and smooth muscle cell proliferation. Circ. Res. 103 (2008), 43–52.
78. [78] Sasaki, M., Kleinman, H.K., Huber, H., Deutzmann, R., Yamada, Y., Laminin, a mulitdomain protein. J. Biol. Chem. 263 (1988), 16536–16544.
79. [79] Haaparanta, T., Uitto, J., Ruoslahti, E., Engvall, E., Molecular cloning of the cDNA encoding human laminin a chain. Matrix 11 (1991), 151–160.
80. [80] Noonan, D.M., Horigan, E.A., Ledbetter, S.R., Vogeli, G., Sasaki, M., Yamada, Y., et al. Identification of cDNA clones encoding different domains of the basement membrane heparan sulfate proteoglycan. J. Biol. Chem. 263 (1988), 16379–16387.
81. [81] Iwata, S., Ito, M., Nakata, T., Noguchi, Y., Okuno, T., Ohkawara, B., et al. A missense mutation in domain III in HSPG2 in Schwartz-Jampel syndrome compromises secretion of perlecan into the extracellular space. Neuromuscul. Disord. 25 (2015), 667–671.
82. [82] Nicole, S., Davoine, C.-S., Topaloglu, H., Cattolico, L., Barral, D., Beighton, P., et al. Perlecan, the major proteoglycan of basement membranes, is altered in patients with Schwartz-Jampel syndrome (chondrodystrophic myotonia). Nat. Genet. 26 (2000), 480–483.
83. [83] Chakravarti, S., Horchar, T., Jefferson, B., Laurie, G.W., Hassell, J.R., Recombinant domain III of perlecan promotes cell attachment through its RGDS sequence. J. Biol. Chem. 270 (1995), 404–409.
84. [84] Cunningham, B.A., Hemperly, J.J., Murray, B.A., Prediger, E.A., Brackenbury, R., Edelman, G.M., Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236 (1987), 799–806.
85. [85] Hopf, M., Göhring, W., Kohfeldt, E., Yamada, Y., Timpl, R., Recombinant domain IV of perlecan binds to nidogens, laminin-nidogen complex, fibronectin, fibulin-2 and heparin. Eur. J. Biochem. 259 (1999), 917–925.
86. [86] Grindel, B., Li, Q., Arnold, R., Petros, J., Zayzafoon, M., Muldoon, M., et al. Perlecan/HSPG2 and matrilysin/MMP-7 as indices of tissue invasion: tissue localization and circulating perlecan fragments in a cohort of 288 radical prostatectomy patients. Oncotarget 7 (2016), 10433–10447.
87. [87] Arpino, V., Brock, M., Gill, S.E., The role of TIMPs in regulation of extracellular matrix proteolysis. Matrix Biol. 44-46 (2015), 247–254.
88. [88] Wells, J.M., Gaggar, A., Blalock, J.E., MMP generated matrikines. Matrix Biol. 44-46 (2015), 122–129.
89. [89] Deryugina, E.I., Quigley, J.P., Tumor angiogenesis: MMP-mediated induction of intravasation- and metastasis-sustaining neovasculature. Matrix Biol. 44-46 (2015), 94–112.
90. [90] Rohani, M.G., Parks, W.C., Matrix remodeling by MMPs during wound repair. Matrix Biol. 44-46 (2015), 113–121.
91. [91] Duarte, S., Baber, J., Fujii, T., Coito, A.J., Matrix metalloproteinases in liver injury, repair and fibrosis. Matrix Biol. 44-46 (2015), 147–156.
92. [92] Eckhard, U., Huesgen, P.F., Schilling, O., Bellac, C.L., Butler, G.S., Cox, J.H., et al. Active site specificity profiling of the matrix metalloproteinase family: proteomic identification of 4300 cleavage sites by nine MMPs explored with structural and synthetic peptide cleavage analyses. Matrix Biol. 49 (2016), 37–60.
93. [93] Gonzalez, E.M., Reed, C.C., Bix, G., Fu, J., Zhang, Y., Gopalakrishnan, B., et al. BMP-1/Tolloid-like metalloproteases process endorepellin, the angiostatic C-terminal fragment of perlecan. J. Biol. Chem. 280 (2005), 7080–7087.
94. [94] Thadikkaran, L., Crettaz, D., Siegenthaler, M.A., Gallot, D., Sapin, V., Iozzo, R.V., et al. The role of proteomics in the assessment of premature rupture of fetal membranes. Clin. Chim. Acta 360 (2005), 27–36.
95. [95] Oda, O., Shinzato, T., Ohbayashi, K., Takai, I., Kunimatsu, M., Maeda, K., et al. Purification and characterization of perlecan fragment in urine of end-stage renal failure patients. Clin. Chim. Acta 255 (1996), 119–132.
96. [96] O'Riordan, E., Orlova, T.N., Mendelev, N., Patschan, D., Kemp, R., Chander, P.N., et al. Urinary proteomic analysis of chronic renal allograft nephropathy. Proteomics Clin. Appl. 2 (2008), 1025–1035.
97. [97] Tsangaris, G.T., Karamessinis, P., Kolialexi, A., Garbis, S.D., Antsaklis, A., Mavrou, A., et al. Proteomic analysis of amniotic fluid in pregnancies with down syndrome. Proteomics 6 (2006), 4410–4419.
98. [98] Chang, J.W., Kang, U.-B., Kim, D.H., Yi, J.K., Lee, J.W., Noh, D.-Y., et al. Identification of circulating endorepellin LG3 fragment: potential use as a serological biomarker for breast cancer. Proteomics Clin. Appl. 2 (2008), 23–32.
99. [99] Pilon, E.A., Dieude, M., Qi, S., Hamelin, K., Pomerleau, L., Beillevaire, D., et al. The perlecan fragment LG3 regulates homing of mesenchymal stem cells and neointima formation during vascular rejection. Am. J. Transplant. 15 (2015), 1205–1218.
100. [100] Dieude, M., Bell, C., Turgeon, J., Beillevaire, D., Pomerleau, L., Yang, B., et al. The 20S proteasome core, active within apoptotic exosome-like vesicles, induces autoantibody production and accelerates rejection. Sci. Transl. Med., 7, 2015 (318ra200).
101. [101] SundarRaj, N., Fite, D., Ledbetter, S., Chakravarti, S., Hassell, J.R., Perlecan is a component of cartilage matrix and promotes chondrocyte attachment. J. Cell Sci. 108 (1995), 2663–2672.
102. [102] Govindraj, P., West, L., Koob, T.J., Neame, P., Doege, K., Hassell, J.R., Isolation and identification of the major heparan sulfate proteoglycans in the developing bovine rib growth plate. J. Biol. Chem. 277 (2002), 19461–19469.
103. [103] Govindraj, P., West, L., Smith, S., Hassell, J.R., Modulation of FGF-2 binding to chondrocytes from the developing growth plate by perlecan. Matrix Biol. 25 (2006), 232–239.
104. [104] Merz, D.C., Alves, G., Kawano, T., Zheng, H., Culotti, J.G., UNC-52/perlecan affects gonadal leader cell migrations in C.elegans hermaphrodites through alterations in growth factor signaling. Dev. Biol. 256 (2003), 173–186.
105. [105] Mullen, G.P., Rogalski, T.M., Bush, J.A., Gorji, P.R., Moerman, D.G., Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol. Biol. Cell 10 (1999), 3205–3221.
106. [106] Rogalski, T.M., Gilchrist, E.J., Mullen, G.P., Moerman, D.G., Mutations in the unc-52 gene responsible for body wall muscle defects in adult Caenorhabditis elegans are located in alternatively spliced exons. Genetics 139 (1995), 159–169.
107. [107] Voigt, A., Pflanz, R., Schafer, U., Jackle, H., Perlecan participates in proliferation activation of quiescent Drosophila neuroblasts. Dev. Dyn. 224 (2002), 403–412.
108. [108] Lindner, J.R., Hillman, P.R., Barrett, A.L., Jackson, M.C., Perry, T.L., Park, Y., et al. The Drosophila perlecan gene trol regulates multiple signaling pathways in different developmental contexts. BMC Dev. Biol., 7, 2007, 121.
109. [109] Park, Y., Rangel, C., Reynolds, M.M., Caldwell, M.C., Johns, M., Nayak, M., et al. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev. Biol. 253 (2003), 247–257.
110. [110] Grigorian, M., Liu, T., Banerjee, U., Hartenstein, V., The proteoglycan trol controls the architecture of the extracellular matrix and balances proliferation and differentiation of blood progenitors in the drosophila lymph gland. Dev. Biol. 384 (2013), 301–312.
111. [111] San Antonio, J.D., Zoeller, J.J., Habursky, K., Turner, K., Pimtong, W., Burrows, M., et al. A key role for the integrin α2β1 in experimental and developmental angiogenesis. Am. J. Pathol. 175 (2009), 1338–1347.
112. [112] Costell, M., Gustafsson, E., Aszódi, A., Mörgelin, M., Bloch, W., Hunziker, E., et al. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 147 (1999), 1109–1122.
113. [113] Costell, M., Carmona, R., Gustafsson, E., González-Iriarte, M., Fässler, R., Munoz-Chápuli, R., Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecan-null mice. Circ. Res. 91 (2002), 158–164.
114. [114] Arikawa-Hirasawa, E., Watanabe, E., Takami, H., Hassell, J.R., Yamada, Y., Perlecan is essential for cartilage and cephalic development. Nat. Genet. 23 (1999), 354–358.
115. [115] Pan, Y., Carbe, C., Kupich, S., Pickhinke, U., Ohlig, S., Frye, M., et al. Heparan sulfate expression in the neural crest is essential for mouse cardiogenesis. Matrix Biol. 35 (2014), 253–265.
116. [116] Rossi, M., Morita, H., Sormunen, R., Airenne, S., Kreivi, M., Wang, L., et al. Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22 (2003), 236–245.
117. [117] Inomata, T., Ebihara, N., Funaki, T., Matsuda, A., Wantanabe, Y., Ning, L., et al. Perlecan-deficient mutation impairs corneal epithelial structure. Invest. Ophthalmol. Vis. Sci. 53 (2012), 1277–1284.
118. [118] Tran, P.-K., Tran-Lundmark, K., Soininen, R., Tryggvason, K., Thyberg, J., Hedin, U., Increased intimal hyperplasia and smooth muscle cell proliferation in transgenic mice with heparan sulfate-deficient perlecan. Circ. Res. 94 (2004), 550–558.
119. [119] Zhou, Z., Wang, J., Cao, R., Morita, H., Soininen, R., Chan, K.M., et al. Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice. Cancer Res. 64 (2004), 4699–4702.
120. [120] Nonaka, R., Iesaki, T., de Vega, S., Daida, H., Okada, T., Sasaki, T., et al. Perlecan deficiency causes endothelial dysfunction by reducing the expression of endothelial nitric oxide synthase. Phys. Rep., 3, 2015, e12272.
121. [121] Arikawa-Hirasawa, E., Wilcox, W.R., Le, A.H., Silverman, N., Govindraj, P., Hassell, J.R., et al. Dyssegmental dysplasia, Silverman-Handmaker type, is caused by functional null mutations of the perlecan gene. Nat. Genet. 27 (2001), 431–434.
122. [122] Arikawa-Hirasawa, E., Le, A.H., Nishino, I., Nonaka, I., Ho, N.C., Francomano, C.A., et al. Structural and functional mutations of the perlecan gene cause Schwartz-Jampel syndrome, with myotonic myopathy and chondrodysplasia. Am. J. Hum. Genet. 70 (2002), 1368–1375.
123. [123] Arikawa-Hirasawa, E., Wilcox, W.R., Yamada, Y., Dyssegmental dysplasia, Silverman-Handmaker type: unexpected role of perlecan in cartilage development. Am. J. Med. Genet. 106 (2001), 254–257.
124. [124] Cartaud, A., Strochlic, L., Guerra, M., Blanchard, B., Lambergeon, M., Krejci, E., et al. MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction. J. Cell Biol. 165 (2004), 505–515.
125. [125] Peng, H.B., Xie, H., Rossi, S.G., Rotundo, R.L., Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J. Cell Biol. 145 (1999), 911–921.
126. [126] Neill, T., Schaefer, L., Iozzo, R.V., Decoding the matrix: instructive roles of proteoglycan receptors. Biochemistry 54 (2015), 4583–4598.
127. [127] Arikawa-Hirasawa, E., Rossi, S.G., Rotundo, R.L., Yamada, Y., Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat. Neurosci. 5 (2002), 119–123.
128. [128] Willis, C.D., Schaefer, L., Iozzo, R.V., The biology of perlecan and its bioactive modules. Karamanos, N.K., (eds.) Extracellular Matrix: Pathobiology and Signaling, 2012, Walter de Gruyter GmbH & Co. KG, Berlin, 171–184.
129. [129] Woodall, B.P., Nyström, A., Iozzo, R.A., Eble, J.A., Niland, S., Krieg, T., et al. Integrin α2β1 is the required receptor for endorepellin angiostatic activity. J. Biol. Chem. 283 (2008), 2335–2343.
130. [130] Aviezer, D., Hecht, D., Safran, M., Eisinger, M., David, G., Yayon, A., Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell 79 (1994), 1005–1013.
131. [131] Zoeller, J.J., Whitelock, J., Iozzo, R.V., Perlecan regulates developmental angiogenesis by modulating the VEGF-VEGFR2 axis. Matrix Biol. 28 (2009), 284–291.
132. [132] Kaji, T., Yamamoto, C., Oh-i, M., Fujiwara, Y., Yamazaki, Y., Morita, T., et al. The vascular endothelial growth factor VEGF165 induces perlecan synthesis via VEGF receptor-2 in cultured human brain microvascular endothelial cells. Biochim. Biophys. Acta 1760 (2006), 1465–1474.
133. [133] Chuang, C.Y., Lord, M.S., Melrose, J., Rees, M.D., Knox, S.M., Freeman, C., et al. Heparan sulfate-dependent signaling of fibroblast growth growth factor 18 by chondrocyte-derived perlecan. Biochemistry 49 (2010), 5524–5532.
134. [134] Bix, G., Iozzo, R.V., Matrix revolutions: “tails” of basement-membrane components with angiostatic functions. Trends Cell Biol. 15 (2005), 52–60.
135. [135] Bix, G., Iozzo, R.V., Novel interactions of perlecan: unraveling perlecan's role in angiogenesis. Microsc. Res. 71 (2008), 339–348.
136. [136] Goyal, A., Pal, N., Concannon, M., Paulk, M., Doran, M., Poluzzi, C., et al. Endorepellin, the angiostatic module of perlecan, interacts with both the α2β1 integrin and vascular endothelial growth factor receptor 2 (VEGFR2). J. Biol. Chem. 286 (2011), 25947–25962.
137. [137] Bix, G., Fu, J., Gonzalez, E., Macro, L., Barker, A., Campbell, S., et al. Endorepellin causes endothelial cell disassembly of actin cytoskeleton and focal adhesions through the α2β1 integrin. J. Cell Biol. 166 (2004), 97–109.
138. [138] Willis, C.D., Poluzzi, C., Mongiat, M., Iozzo, R.V., Endorepellin laminin-like globular repeat 1/2 domains bind Ig3-5 of vascular endothelial growth factor(VEGF) receptor 2 and block pro-angiogenic signaling by VEGFA in endothelial cells. FEBS J. 280 (2013), 2271–2294.
139. [139] Bix, G., Iozzo, R.A., Woodall, B., Burrows, M., McQuillan, A., Campbell, S., et al. Endorepellin, the C-terminal angiostatic module of perlecan, enhances collagen-platelet responses via the α2β1 integrin receptor. Blood 109 (2007), 3745–3748.
140. [140] Nyström, A., Shaik, Z.P., Gullberg, D., Krieg, T., Eckes, B., Zent, R., et al. Role of tyrosine phosphatase SHP-1 in the mechanism of endorepellin angiostatic activity. Blood 114 (2009), 4897–4906.
141. [141] Goyal, A., Poluzzi, C., Willis, A.C., Smythies, J., Shellard, A., Neill, T., et al. Endorepellin affects angiogenesis by antagonizing diverse VEGFR2- evoked signaling pathways: transcriptional repression of HIF-1α and VEGFA and concurrent inhibition of NFAT1 activation. J. Biol. Chem. 287 (2012), 43543–43556.
142. [142] Bhattacharya, R., Kwon, J., Wang, E., Mukherjee, P., Mukhopadhyay, D., Src homology 2 (SH2) domain containing protein tyrosine phosphatase-1 (SHP-1) dephosphorylates VEGF receptor-2 and attenuates endothelial DNA synthesis, but not migration. J. Mol. Signal., 3, 2008, 8.
143. [143] Choi, A.M.K., Ryter, S.W., Levine, B., Autophagy in human health and disease. New Engl. J. Med. 368 (2013), 651–662.
144. [144] Goyal, A., Gubbiotti, M.A., Chery, D.R., Han, L., Iozzo, R.V., Endorepellin-evoked autophagy contributes to angiostasis. J. Biol. Chem., 2016 In press.
145. [145] Thoreen, C.C., Kang, S.A., Chang, J.W., Liu, Q., Zhang, J., Gao, Y., et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284 (2009), 8023–8032.
146. [146] Vigetti, D., Viola, M., Karousou, E., De, L.G., Passi, A., Metabolic control of hyaluronan synthases. Matrix Biol. 35 (2014), 8–13.
147. [147] Hascall, V.C., Wang, A., Tammi, M., Oikari, S., Tammi, R., Passi, A., et al. The dynamic metabolism of hyaluronan regulates the cytosolic concentration of UDP-GlcNAc. Matrix Biol. 35 (2014), 14–17.
148. [148] Wang, A., Sankaranarayanan, N.V., Yanagishita, M., Templeton, D.M., Desai, U.R., Sugahara, K., et al. Heparin interaction with a receptor on hyperglycemic dividing cells prevents intracellular hyaluronan synthesis and autophagy responses in models of type 1 diabetes. Matrix Biol. 48 (2015), 36–41.
149. [149] Vigetti, D., Clerici, M., Deleonibus, S., Karousou, E., Viola, M., Moretto, P., et al. Hyaluronan synthesis is inhibited by adenosine monophosphate-activated protein kinase through the regulation of HAS2 activity in human aortic smooth muscle cells. J. Biol. Chem. 286 (2011), 7917–7924.
150. [150] Bix, G., Castello, R., Burrows, M., Zoeller, J.J., Weech, M., Iozzo, R.A., et al. Endorepellin in vivo: targeting the tumor vasculature and retarding cancer growth and metabolism. J. Natl. Cancer Inst. 98 (2006), 1634–1646.
151. [151] Nguyen, T.M.B., Subramanian, I.V., Xiao, X., Ghosh, G., Nguyen, P., Kelekar, A., et al. Endostatin induces autophagy in endothelial cells by modulating Beclin 1 and β-catenin levels. J. Cell. Mol. Med. 13 (2009), 3687–3698.
152. [152] Järveläinen, H., Sainio, A., Wight, T.N., Pivotal role for decorin in angiogenesis. Matrix Biol. 43 (2015), 15–26.
153. [153] Buraschi, S., Neill, T., Goyal, A., Poluzzi, C., Smythies, J., Owens, R.T., et al. Decorin causes autophagy in endothelial cells via Peg3. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), E2582–E2591.
154. [154] Neill, T., Torres, A.T., Buraschi, S., Iozzo, R.V., Decorin has an appetite for endothelial cell autophagy. Autophagy 9 (2013), 1626–1628.
155. [155] Neill, T., Schaefer, L., Iozzo, R.V., Decorin, a guardian from the matrix. Am. J. Pathol. 181 (2012), 380–387.
156. [156] Neill, T., Torres, A., Buraschi, S., Owens, R.T., Hoek, J., Baffa, R., et al. Decorin induces mitophagy in breast carcinoma cells via peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) and mitostatin. J. Biol. Chem. 289 (2014), 4952–4968.
157. [157] Gubbiotti, M.A., Neill, T., Frey, H., Schaefer, L., Iozzo, R.V., Decorin is an autophagy-inducible proteoglycan and is required for proper in vivo autophagy. Matrix Biol. 48 (2015), 14–25.
158. [158] Gubbiotti, M.A., Iozzo, R.V., Proteoglycans regulate autophagy via outside-in signaling: an emerging new concept. Matrix Biol. 48 (2015), 6–13.
159. [159] Myren, M., Kirby, D.J., Noonan, M.L., Maeda, A., Owens, R.T., Ricard-Blum, S., et al. Biglycan potentially regulates angiogenesis during fracture repair by altering expression and function of endostatin. Matrix Biol. 52-54 (2016), 141–150.
160. [160] Carmignac, V., Svensson, M., Körner, Z., Elowsson, L., Matsumura, C., Gawlik, K.I., et al. Autophagy is increased in laminin α2 chain-deficient muscle and its inhibition improves muscle morphology in a mouse model of MDC1A. Hum. Mol. Genet. 20 (2011), 4891–4902.