Proteoglycans regulate autophagy via outside-in signaling: An emerging new concept

Matrix Biology

Volumn 48, Issue , 2015, Pages 6-13

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

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DECORIN; ENDOREPELLIN; FIBROBLAST GROWTH FACTOR 2; PERLECAN; PROTEOGLYCAN; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; DCN PROTEIN, HUMAN; ENDOREPELLIN PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; PEPTIDE FRAGMENT; PROTEOHEPARAN SULFATE;

ANGIOGENESIS; AUTOPHAGOSOME; AUTOPHAGY; BASEMENT MEMBRANE; CARCINOGENESIS; ENDOTHELIUM CELL; MITOCHONDRION; MITOPHAGY; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; NOTE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CYTOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOUSE; REPORTER GENE; TRANSGENIC MOUSE;

ANIMALS; AUTOPHAGY; DECORIN; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 84947728400     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2015.10.002     Document Type: Note

References (84)

1. He C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 2009, 43:67-93.
2. Murrow L., Debnath J. Autophagy as a stress-response and quality-control mechanism: implications for cell injury and human disease. Annu. Rev. Pathol. 2013, 8:105-137.
3. Lum J.J., Bauer D.E., Kong M., Harris M.H., Li C., Lindsten T., et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 2005, 120:237-248.
4. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 2004, 6:1221-1228.
5. Choi A.M.K., Ryter S.W., Levine B. Autophagy in human health and disease. New Engl. J. Med. 2013, 368:651-662.
6. Grumati P., Coletto L., Sabatelli P., Cescon M., Angelin A., Bertaggia E., et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat. Med. 2011, 16:1313-1320.
7. Grumati P., Bonaldo P. Autophagy in skeletal muscle homeostasis and in muscular dystrophies. Cells 2012, 1:325-345.
8. Rabinowitz J.D., White E. Autophagy and metabolism. Science 2010, 330:1344-1348.
9. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64.
10. Karsli-Uzunbas G., Guo J.Y., Price S., Teng X., Laddha S.V., Khor S., et al. Autophagy is required for glucose homeostasis and lung tumor maintenance. Cancer Discov. 2014, 4:914-927.
11. Morselli E., Galluzzi L., Kepp O., Marino G., Michaud M., Vitale I., et al. Oncosuppressive functions of autophagy. Antioxid. Redox Signal. 2011, 14:2251-2269.
12. 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. 2013, 110:E2582-E2591.
13. Goyal A., Neill T., Owens R.T., Schaefer L., Iozzo R.V. Decorin activates AMPK, an energy sensor kinase, to induce autophagy in endothelial cells. Matrix Biol. 2014, 34:46-54.
14. Poluzzi C., Casulli J., Goyal A., Mercer T.J., Neill T., Iozzo R.V. Endorepellin evokes autophagy in endothelial cells. J. Biol. Chem. 2014, 289:16114-16128.
15. Neill T., Torres A.T., Buraschi S., Iozzo R.V. Decorin has an appetite for endothelial cell autophagy. Autophagy 2013, 9:1626-1628.
16. Nguygen T.M.B., Subramanian I.V., Kelekar A., Ramakrishnan S. Kringle 5 of human plasminogen, an angiogenesis inhibitor, induces both autophagy and apoptotic death in endothelial cells. Blood 2007, 109:4793-4802.
17. 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. 2011, 20:4891-4902.
18. Chau Y.-P., Lin J.-Y., Chen J.H.-C., Tai M.-H. Endostatin induces autophagic cell death in EAhy926 human endothelial cells. Histol. Histopathol. 2003, 18:715-726.
19. Neill T., Schaefer L., Iozzo R.V. Decoding the matrix: instructive roles of proteoglycan receptors. Biochemistry 2015, 54:4583-4598.
20. Neill T., Schaefer L., Iozzo R.V. Decorin, a guardian from the matrix. Am. J. Pathol. 2012, 181:380-387.
21. Chen S., Young M.F., Chakravarti S., Birk D.E. Interclass small leucine-rich repeat proteoglycan interactions regulate collagen fibrillogenesis and corneal stromal assembly. Matrix Biol. 2014, 35:103-111.
22. Dunkman A.A., Buckley M.R., Mienaltowski M.J., Adams.S.M., thomas S.J., satchell L., et al. Decorin expression is important for age-related changes in tendon structure and mechanical properties. Matrix Biol. 2013, 32:3-13.
23. Reese S.P., Underwood C.J., Weiss J.A. Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Biol. 2013, 32:414-423.
24. Dunkman A.A., Buckley M.R., Mienaltowski M.J., Adams S.M., Thomas S.J., Kumar A., et al. The injury response of aged tendons in the absence of biglycan and decorin. Matrix Biol. 2014, 35:232-238.
25. Neill T., Painter H., Buraschi S., Owens R.T., Lisanti M.P., Schaefer L., et al. Decorin antagonizes the angiogenic network. Concurrent inhibition of met, hypoxia inducible factor-1α and vascular endothelial growth factor a and induction of thrombospondin-1 and TIMP3. J. Biol. Chem. 2012, 287:5492-5506.
26. Järveläinen H., Saino A., Wight T.N. Pivotal role for decorin in angiogenesis. Matrix Biol. 2015, 43:15-26.
27. De Luca A., Santra M., Baldi A., Giordano A., Iozzo R.V. Decorin-induced growth suppression is associated with upregulation of p21, an inhibitor of cyclin-dependent kinases. J. Biol. Chem. 1996, 271:18961-18965.
28. Buraschi S., Pal N., Tyler-Rubinstein N., Owens R.T., Neill T., Iozzo R.V. Decorin antagonizes met receptor activity and downregulates β-catenin and Myc levels. J. Biol. Chem. 2010, 285:42075-42085.
29. 2+ in A431 cells. J. Biol. Chem. 1998, 273:3121-3124.
30. Brandan E., Gutierrez J. Role of skeletal muscle proteoglycans during myogenesis. Matrix Biol. 2013, 32:289-297.
31. Fetting J.L., Guay J.A., Karolak M.J., Iozzo R.V., Adams D.C., Maridas D.E., et al. FOXD1 promotes nephron progenitor differentiation by repressing decorin in the embryonic kidney. Development 2014, 141:17-27.
32. Nikolovska K., Renke J.K., Jungmann O., Grobe K., Iozzo R.V., Zamfir A.D., et al. A decorin-deficient matrix affects skin chondroitin/dermatan sulfate levels and keratinocyte function. Matrix Biol. 2014, 35:91-102.
33. Morcavallo A., Buraschi S., Xu S.-Q., Belfiore A., Schaefer L., Iozzo R.V., et al. Decorin differentially modulates the activity of insulin receptor isoform a ligands. Matrix Biol. 2014, 35:82-90.
34. Horvath Z., Kovalszky I., Fullar A., Kiss K., Schaff Z., Iozzo R.V., et al. Decorin deficiency promotes hepatic carcinogenesis. Matrix Biol. 2014, 35:194-205.
35. Skandalis S.S., Afratis N., Smirlaki G., Nikitovic D., Theocharis A.D., Tzanakakis G.N., et al. Cross-talk between estradiol receptor and EGFR/IGF-IR signaling pathways in estrogen-responsive breast cancers: focus on the role and impact of proteoglycans. Matrix Biol. 2014, 35:182-193.
36. Wu Z., Horgan C.E., Carr O., Owens R.T., Iozzo R.V., Lechner B.E. Biglycan and decorin differentially regulate signaling in the fetal membranes. Matrix Biol. 2014, 35:266-275.
37. Duncan M.B. Extracellular matrix transcriptome dynamics in hepatocellular carcinoma. Matrix Biol. 2013, 32:393-398.
38. Grant D.S., Yenisey C., Rose R.W., Tootell M., Santra M., Iozzo R.V. Decorin suppresses tumor cell-mediated angiogenesis. Oncogene 2002, 21:4765-4777.
39. Neill T., Jones H.R., Crane-Smith Z., Owens R.T., Schaefer L., Iozzo R.V. Decorin induces rapid secretion of thrombospondin-1 in basal breast carcinoma cells via inhibition of ras homolog gene family, member a/rho-associated coiled-coil containing protein kinase 1. FEBS J. 2013, 280:2353-2368.
40. Ferrara N., Gerber H.-P., LeCouter J. The biology of VEGF and its receptors. Nat. Med. 2003, 9:669-676.
41. Murphy-Ullrich J.E., Sage E.H. Revisiting the matricellular concept. Matrix Biol. 2014, 37:1-14.
42. Wallace D.M., Murphy-Ullrich J.E., Downs J.C., O'Brien C.J. The role of matricellular proteins in glaucoma. Matrix Biol. 2014, 37:174-182.
43. Resovi A., Pinessi D., Chiorino G., Taraboletti G. Current understanding of the thrombospondin-1 interactome. Matrix Biol. 2014, 37:83-91.
44. Rogers N.M., Sharifi-Sanjani M., Csanyi G., Pagano P.J., Isenberg J.S. Thrombospondin-1 and CD47 regulation of cardiac, pulmonary and vascular responses in health and disease. Matrix Biol. 2014, 37:92-101.
45. Duquette M., Nadler M., Okuhara D., Thompson J., Shuttleworth T., Lawler J. Members of the thrombospondin gene family bind stromal interaction molecule 1 and regulate calcium channel activity. Matrix Biol. 2014, 37:15-24.
46. Soto-Pantoja D.R., Shih H.B., Maxhimer J.B., Cook K.L., Ghosh A., Isenberg J.S., et al. Thrombospondin-1 and CD47 signaling regulate healing of thermal injury in mice. Matrix Biol. 2014, 37:25-34.
47. Miller T.W., Kaur S., Ivins-O'Keefe K., Roberts D.D. Thrombospondin-1 is a CD47-dependent endogenous inhibitor of hydrogen sulfide signaling in T cell activation. Matrix Biol. 2013, 32:316-324.
48. Neill T, Schaefer L, Iozzo RV. An oncosuppressive role for decorin. Mol. Cell Oncol. 2015;2:e975645.
49. Buraschi S., Neill T., Owens R.T., Iniguez L.A., Purkins G., Vadigepalli R., et al. Decorin protein core affects the global gene expression profile of the tumor microenvironment in a triple-negative orthotopic breast carcinoma xenograft model. PLoS One 2012, 7.
50. 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. 2014, 289:4952-4968.
51. Fassan M., D'Arca D., Letko J., Vecchione A., Gardiman M.P., McCue P., et al. Mitostatin is down-regulated in human prostate cancer and suppresses the invasive phenotype of prostate cancer cells. PLoS One 2011, 6.
52. Vecchione A., Fassan M., Anesti V., Morrione A., Goldoni S., Baldassarre G., et al. Mitostatin, a putative tumor suppressor on chromosome 12q24.1, is downregulated in human bladder and breast cancer. Oncogene 2009, 28:257-269.
53. 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 2015, 48:14-25.
54. 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. 2014, 35:112-122.
55. 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. 2008, 181:381-394.
56. Zoeller J.J., Whitelock J., Iozzo R.V. Perlecan regulates developmental angiogenesis by modulating the VEGF-VEGFR2 axis. Matrix Biol. 2009, 28:284-291.
57. 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. 2014, 34:64-79.
58. 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. 2013, 32:178-187.
59. 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. 2001, 27:431-434.
60. Arikawa-Hirasawa E., Wilcox W.R., Yamada Y. Dyssegmental dysplasia, silverman-handmaker type: unexpected role of perlecan in cartilage development. Am. J. Med. Genet. 2001, 106:254-257.
61. Iozzo R.V. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 2005, 6:646-656.
62. Iozzo R.V., Zoeller J.J., Nyström A. Basement membrane proteoglycans: modulators par excellence of cancer growth and angiogenesis. Mol. Cells 2009, 27:503-513.
63. 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 2015, 48:26-35.
64. Iozzo R.V., Sanderson R.D. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 2011, 15:1013-1031.
65. Bix G., Iozzo R.V. Novel interactions of perlecan: unraveling perlecan's role in angiogenesis. Microsc. Res. 2008, 71:339-348.
66. 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. 2003, 278:4238-4249.
67. 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. 2008, 283:2335-2343.
68. 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 2007, 109:3745-3748.
69. 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. 2012, 287:43543-43556.
70. 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. 2006, 98:1634-1646.
71. 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. 2009, 13:3687-3698.
72. Neill T., Schaefer L., Iozzo R.V. Instructive roles of extracellular matrix on autophagy. Am. J. Pathol. 2014, 184:2146-2153.
73. Vlodavsky I., Iozzo R.V., Sanderson R.D. Heparanase: multiple functions in inflammation, diabetes and atherosclerosis. Matrix Biol. 2013, 32:220-222.
74. Parish C.R., Freeman C., Ziolkowski A.F., He Y.Q., Sutcliffe E.L., Zafar A., et al. Unexpected new roles for heparanase in Type 1 diabetes and immune gene regulation. Matrix Biol. 2013, 32:228-233.
75. Vlodavsky I., Blich M., Li J.P., Sanderson R.D., Ilan N. Involvement of heparanase in atherosclerosis and other vessel wall pathologies. Matrix Biol. 2013, 32:241-251.
76. Peterson S.B., Liu J. Multi-faceted substrate specificity of heparanase. Matrix Biol. 2013, 32:223-227.
77. Goldberg R., Meirovitz A., Hirshoren N., Bulvik R., Binder A., Rubinstein A.M., et al. Versatile role of heparanase in inflammation. Matrix Biol. 2013, 32:234-240.
78. Shteingauz A., Boyango I., Naroditsky I., Hammond E., Gruber M., Doweck I., et al. Heparanase enhances tumor growth and chemoresistance by promoting autophagy. Cancer Res. 2015, 75:3946-3957.
79. Barash U., Cohen-Kaplan V., Dowek I., Ilan N., Vlodawsky I. Proteoglycans in health and disease: new concepts for heparanase function in tumor progression and metastasis. FEBS J. 2010, 277:3890-3903.
80. Mahtouk K., Hose D., Raynaud P., Hundemer M., Jourdan M., Jourdan E., et al. Heparanase influences expression and shedding of syndecan-1, and its expression by the bone marrow environment is a bad prognostic factor in multiple myeloma. Blood 2007, 109:4914-4923.
81. Purushothaman A., Uyama T., Kobayashi F., Yamada S., Sugahara K., Rapraeger A.C., et al. Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endothelial invasion and angiogenesis. Blood 2010, 115:2449-2457.
82. Purushothaman A., Hurst D.R., Pisano C., Mizumoto S., Sugahara K., Sanderson R.D. Heparanase-mediated loss of nuclear syndecan-1 enhances histone acetyltransferase (HAT) activity to promote expression of genes that drive an aggressive tumor phenotype. J. Biol. Chem. 2011, 286:30377-30383.
83. Sanderson R.D., Yang Y., Suva L.J., Kelly T. Heparan sulfate proteoglycans and heparanase - partners in osteolytic tumor growth and metastasis. Matrix Biol. 2004, 23:341-352.
84. Thompson C.A., Purushothaman A., Ramani V.C., Vlodavsky I., Sanderson R.D. Heparanase regulates secretion, composition, and function of tumor cell-derived exosomes. J. Biol. Chem. 2013, 288:10093-10099.