Stress-induced ECM alteration modulates cellular microRNAs that feedback to readjust the extracellular environment and cell behavior

Frontiers in Genetics

Volumn 4, Issue DEC, 2013, Pages

  Edeleva, Evgeniia V ^a   Shcherbata, Halyna R ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Bi directional signal transduction; Dystroglycan; ECM composition; Extrinsic stress; MiRNAs

Indexed keywords

EID: 84892419197     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00305     Document Type: Review

References (81)

1. Alessi, A., Bragg, A. D., Percival, J. M., Yoo, J., Albrecht, D. E., Froehner, S. C., et al. (2006). gamma-Syntrophin scaffolding is spatially and functionally distinct from that of the alpha/beta syntrophins. Exp. Cell Res. 312, 3084-3095. doi: 10.1016/j.yexcr.2006.06.019.
2. Ariel, A., Hershkoviz, R., Cahalon, L., Williams, D. E., Akiyama, S. K., Yamada, K. M., et al. (1997). Induction of T cell adhesion to extracellular matrix or endothelial cell ligands by soluble or matrix-bound interleukin-7. Eur. J. Immunol. 27, 2562-2570. doi: 10.1002/eji.1830271015.
3. Barresi, R., and Campbell, K. P. (2006). Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119, 199-207. doi: 10.1242/jcs.02814.
4. Bhat, H. F., Adams, M. E., and Khanday, F. A. (2013). Syntrophin proteins as Santa Claus: role(s) in cell signal transduction. Cell. Mol. Life Sci. 70, 2533-2554. doi: 10.1007/s00018-012-1233-9.
5. Bissell, M. J., Hall, H. G., and Parry, G. (1982). How does the extracellular matrix direct gene expression? J. Theor. Biol. 99, 31-68. doi: 10.1016/0022-5193(82)90388-5.
6. Cacchiarelli, D., Martone, J., Girardi, E., Cesana, M., Incitti, T., Morlando, M., et al. (2010). MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway. Cell Metab. 12, 341-351. doi: 10.1016/j.cmet.2010.07.008.
7. Campbell, K. P. (1995). Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80, 675-679. doi: 10.1016/0092-8674(95)90344-5.
8. Castoldi, G., Di Gioia, C. R. T., Bombardi, C., Catalucci, D., Corradi, B., Gualazzi, M. G., et al. (2012). MiR-133a regulates collagen 1A1: potential role of miR-133a in myocardial fibrosis in angiotensin II-dependent hypertension. J. Cell. Physiol. 227, 850-856. doi: 10.1002/jcp.22939.
9. Chawla, G., and Sokol, N. S. (2012). Hormonal activation of let-7-C microRNAs via EcR is required for adult Drosophila melanogaster morphology and function. Development 139, 1788-1797. doi: 10.1242/dev.077743.
10. Choi, I. K., and Hyun, S. (2012). Conserved microRNA miR-8 in fat body regulates innate immune homeostasis in Drosophila. Dev. Comp. Immunol. 37, 50-54. doi: 10.1016/j.dci.2011.12.008.
11. Chuang, C. Y., Lord, M. S., Melrose, J., Rees, M. D., Knox, S. M., Freeman, C., et al. (2010). Heparan sulfate-dependent signaling of fibroblast growth factor 18 by chondrocyte-derived perlecan. Biochemistry 49, 5524-5532. doi: 10.1021/bi1005199.
12. Cohn, R. D. (2005). Dystroglycan: important player in skeletal muscle and beyond. Neuromuscul. Disord. 15, 207-217. doi: 10.1016/j.nmd.2004.11.005.
13. Corsten, M. F., Dennert, R., Jochems, S., Kuznetsova, T., Devaux, Y., Hofstra, L., et al. (2010). Circulating MicroRNA-208b and MicroRNA-499 reflect myocardial damage in cardiovascular disease. Circ. Cardiovasc. Genet. 3, 499-506. doi: 10.1161/CIRCGENETICS.110.957415.
14. Côté, P. D., Moukhles, H., and Carbonetto, S. (2002). Dystroglycan is not required for localization of dystrophin, syntrophin, and neuronal nitric-oxide synthase at the sarcolemma but regulates integrin alpha 7B expression and caveolin-3 distribution. J. Biol. Chem. 277, 4672-4679. doi: 10.1074/jbc.M106879200.
15. De Rosa, S., Fichtlscherer, S., Lehmann, R., Assmus, B., Dimmeler, S., and Zeiher, A. M. (2011). Transcoronary concentration gradients of circulating microRNAs. Circulation 124, 1936-1944. doi: 10.1161/CIRCULATIONAHA.111.037572.
16. Gabriely, G., Wurdinger, T., Kesari, S., Esau, C. C., Burchard, J., Linsley, P. S., et al. (2008). MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol. Cell. Biol. 28, 5369-5380. doi: 10.1128/MCB.00479-08.
17. Gandellini, P., Profumo, V., Casamichele, A., Fenderico, N., Borrelli, S., Petrovich, G., et al. (2012). miR-205 regulates basement membrane deposition in human prostate: implications for cancer development. Cell Death Differ. 19, 1750-1760. doi: 10.1038/cdd.2012.56.
18. Garbuzov, A., and Tatar, M. (2010) Hormonal regulation of Drosophila microRNA let-7 and miR-125 that target innate immunity. Fly (Austin) 4, 306-311. doi: 10.4161/fly.4.4.13008.
19. Gerson, K. D., Shearstone, J. R., Maddula, V. S. R. K., Seligmann, B. E., and Mercurio, A. M. (2012). Integrin β 4 regulates SPARC protein to promote invasion. J. Biol. Chem. 287, 9835-9844. doi: 10.1074/jbc.M111.317727.
20. Giancotti, F. G. (1999). Integrin signaling. Science 285, 1028-1033. doi: 10.1126/science.285.5430.1028.
21. Goddeeris, M. M., Wu, B., Venzke, D., Yoshida-Moriguchi, T., Saito, F., Matsumura, K., et al. (2013). LARGE glycans on dystroglycan function as a tunable matrix scaffold to prevent dystrophy. Nature 503, 136-140. doi: 10.1038/nature12605.
22. Guess, C. M., and Quaranta, V. (2009). Defining the role of laminin-332 in carcinoma. Matrix Biol. 28, 445-455. doi: 10.1016/j.matbio.2009.07.008.
23. Hatfield, S. D., Shcherbata, H. R., Fischer, K. A., Nakahara, K., Carthew, R. W., and Ruohola-Baker, H. (2005). Stem cell division is regulated by the microRNA pathway. Nature 435, 974-978. doi: 10.1038/nature03816.
24. He, L., and Hannon, G. J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531. doi: 10.1038/nrg1379.
25. Hergenreider, E., Heydt, S., Tréguer, K., Boettger, T., Horrevoets, A. J. G., Zeiher, A. M., et al. (2012). Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14, 249-256. doi: 10.1038/ncb2441.
26. Hershkoviz, R., Cahalon, L., Miron, S., Alon, R., Sapir, T., Akiyama, S. K., et al. (1994). TNF-alpha associated with fibronectin enhances phorbol myristate acetate-or antigen-mediated integrin-dependent adhesion of CD4+ T cells via protein tyrosine phosphorylation. J. Immunol. 153, 554-565.
27. Hildebrand, A., Romarís, M., Rasmussen, L. M., Heinegård, D., Twardzik, D. R., Border, W. A., et al. (1994). Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem. J. 302, 527-534.
28. Inukai, S., and Slack, F. (2013). MicroRNAs and the genetic network in aging. J. Mol. Biol. 425, 3601-3608. doi: 10.1016/j.jmb.2013.01.023.
29. Ishai-Michaeli, R., Eldor, A., and Vlodavsky, I. (1990). Heparanase activity expressed by platelets, neutrophils, and lymphoma cells releases active fibroblast growth factor from extracellular matrix. Cell Regul. 1, 833-842.
30. Jin, H., Kim, V. N., and Hyun, S. (2012). Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev. 26, 1427-1432. doi: 10.1101/gad.192872.112.
31. Keely, P., Parise, L., and Juliano, R. (1998). Integrins and GTPases in tumour cell growth, motility and invasion. Trends Cell Biol. 8, 101-106. doi: 10.1016/S0962-8924(97)01219-1.
32. Kim, M. J., Cotman, S. L., Halfter, W., and Cole, G. J. (2003). The heparan sulfate proteoglycan agrin modulates neurite outgrowth mediated by FGF-2. J. Neurobiol. 55, 261-277. doi: 10.1002/neu.10213.
33. Kleinman, H. K., and Martin, G. R. (2005). Matrigel: basement membrane matrix with biological activity. Semin. Cancer Biol. 15, 378-386. doi: 10.1016/j.semcancer.2005.05.004.
34. Kucherenko, M. M., Barth, J., Fiala, A., and Shcherbata, H. R. (2012). Steroid-induced microRNA let-7 acts as a spatio-temporal code for neuronal cell fate in the developing Drosophila brain. EMBO J. 31, 4511-4523. doi: 10.1038/emboj.2012.298.
35. Kucherenko, M. M., Marrone, A. K., Rishko, V. M., Magliarelli, H. de. F., and Shcherbata, H. R. (2011). Stress and muscular dystrophy: a genetic screen for dystroglycan and dystrophin interactors in Drosophila identifies cellular stress response components. Dev. Biol. 352, 228-242. doi: 10.1016/j.ydbio.2011.01.013.
36. Kucherenko, M. M., and Shcherbata, H. R. (2013). Steroids as external temporal codes act via miRNAs and cooperate with cytokines in differential neurogenesis. Fly (Austin) 7, 8-7. doi: 10.4161/fly.25241.
37. Larraín, J., Bachiller, D., Lu, B., Agius, E., Piccolo, S., and De Robertis, E. M. (2000). BMP-binding modules in chordin: a model for signalling regulation in the extracellular space. Development 127, 821-830.
38. Li, L.-N., Wang, D.-R., Sato, M., Kojima, N., Imai, K., Higashi, N., et al. (2003). Extracellular matrix-regulated p53 expression and nuclear localization in cultured Detroit 562 cells derived from pharyngeal carcinoma. Arch. Histol. Cytol. 66, 419-428. doi: 10.1679/aohc.66.419.
39. Liu, C., Kelnar, K., Liu, B., Chen, X., Calhoun-Davis, T., Li, H., et al. (2011). The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat. Med. 17, 211-215. doi: 10.1038/nm.2284.
40. Löffler, D., Brocke-Heidrich, K., Pfeifer, G., Stocsits, C., Hackermüller, J., Kretzschmar, A. K., et al. (2007). Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 110, 1330-1333. doi: 10.1182/blood-2007-03-081133.
41. Luna, C., Li, G., Qiu, J., Epstein, D. L., and Gonzalez, P. (2011). Cross-talk between miR-29 and transforming growth factor-betas in trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 52, 3567-3572. doi: 10.1167/iovs.10-6448.
42. Marrone, A. K., Edeleva, E. V., Kucherenko, M. M., Hsiao, N. H., and Shcherbata, H. R. (2012). Dg-Dys-Syn1 signaling in Drosophila regulates the microRNA profile. BMC Cell Biol. 13:26. doi: 10.1186/1471-2121-13-26.
43. Marrone, A. K., Kucherenko, M. M., Rishko, V. M., and Shcherbata, H. R. (2011a). New dystrophin/dystroglycan interactors control neuron behavior in Drosophila eye. BMC Neurosci. 12:93. doi: 10.1186/1471-2202-12-93.
44. Marrone, A. K., Kucherenko, M. M., Wiek, R., Göpfert, M. C., and Shcherbata, H. R. (2011b). Hyperthermic seizures and aberrant cellular homeostasis in Drosophila dystrophic muscles. Sci. Rep. 1, 47. doi: 10.1038/srep00047.
45. Marrone, A. K., and Shcherbata, H. R. (2011). Dystrophin orchestrates the epigenetic profile of muscle cells via miRNAs. Front. Genet. 2:64. doi: 10.3389/fgene.2011.00064.
46. Mathieu, J., and Ruohola-Baker, H. (2013). Regulation of stem cell populations by microRNAs. Adv. Exp. Med. Biol. 786, 329-351. doi: 10.1007/978-94-007-6621-1_18.
47. Moore, S. A., Saito, F., Chen, J., Michele, D. E., Henry, M. D., Messing, A., et al. (2002). Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418, 422-425. doi: 10.1038/nature00838.
48. Olivieri, F., Antonicelli, R., Capogrossi, M. C., and Procopio, A. D. (2013). Circulating microRNAs (miRs) for diagnosing acute myocardial infarction: an exciting challenge. Int. J. Cardiol. 167, 3028-3029. doi: 10.1016/j.ijcard.2012.11.103.
49. Pasquinelli, A. E., Reinhart, B. J., Slack, F., Martindale, M. Q., Kuroda, M. I., Maller, B., et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89. doi: 10.1038/35040556.
50. Piovan, C., Palmieri, D., Di Leva, G., Braccioli, L., Casalini, P., Nuovo, G., et al. (2012). Oncosuppressive role of p53-induced miR-205 in triple negative breast cancer. Mol. Oncol. 6, 458-472. doi: 10.1016/j.molonc.2012.03.003.
51. Pramanik, D., Campbell, N. R., Karikari, C., Chivukula, R., Kent, O. A., Mendell, J. T., et al. (2011). Restitution of tumor suppressor microRNAs using a systemic nanovector inhibits pancreatic cancer growth in mice. Mol. Cancer Ther. 10, 1470-1480. doi: 10.1158/1535-7163.MCT-11-0152.
52. Price, K. J., Tsykin, A., Giles, K. M., Sladic, R. T., Epis, M. R., Ganss, R., et al. (2012). Matrigel basement membrane matrix influences expression of microRNAs in cancer cell lines. Biochem. Biophys. Res. Commun. 427, 343-348. doi: 10.1016/j.bbrc.2012.09.059.
53. Qi, J., Yu, J.-Y., Shcherbata, H. R., Mathieu, J., Wang, A. J., Seal, S., et al. (2009). microRNAs regulate human embryonic stem cell division. Cell Cycle 8, 3729-3741. doi: 10.4161/cc.8.22.10033.
54. Rapraeger, A. C., Krufka, A., and Olwin, B. B. (1991). Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252, 1705-1708. doi: 10.1126/science.1646484.
55. Rayner, K. J., and Hennessy, E. J. (2013). Extracellular communication via microRNA: lipid particles have a new message. J. Lipid Res. 54, 1174-1181. doi: 10.1194/jlr.R034991.
56. Saksela, O., Moscatelli, D., Sommer, A., and Rifkin, D. B. (1988). Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell Biol. 107, 743-751. doi: 10.1083/jcb.107.2.743.
57. Saksela, O., and Rifkin, D. B. (1990). Release of basic fibroblast growth factor-heparan sulfate complexes from endothelial cells by plasminogen activator-mediated proteolytic activity. J. Cell Biol. 110, 767-775. doi: 10.1083/jcb.110.3.767.
58. Schuppan, D., Schmid, M., Somasundaram, R., Ackermann, R., Ruehl, M., Nakamura, T., et al. (1998). Collagens in the liver extracellular matrix bind hepatocyte growth factor. Gastroenterology 114, 139-152. doi: 10.1016/S0016-5085(98)70642-0.
59. Scott, G. K., Goga, A., Bhaumik, D., Berger, C. E., Sullivan, C. S., and Benz, C. C. (2007). Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J. Biol. Chem. 282, 1479-1486. doi: 10.1074/jbc.M609383200.
60. Scott, G. K., Mattie, M. D., Berger, C. E., Benz, S. C., and Benz, C. C. (2006). Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res. 66, 1277-1281. doi: 10.1158/0008-5472.CAN-05-3632.
61. Selaru, F. M., Olaru, A. V., Kan, T., David, S., Cheng, Y., Mori, Y., et al. (2009). MicroRNA-21 is overexpressed in human cholangiocarcinoma and regulates programmed cell death 4 and tissue inhibitor of metalloproteinase 3. Hepatology 49, 1595-1601. doi: 10.1002/hep.22838.
62. Shcherbata, H. R., Yatsenko, A. S., Patterson, L., Sood, V. D., Nudel, U., Yaffe, D., et al. (2007). Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J. 26, 481-493. doi: 10.1038/sj.emboj.7601503.
63. Shi, X.-B., Tepper, C. G., and deVere White, R. W. (2008). Cancerous miRNAs and their regulation. Cell Cycle 7, 1529-1538. doi: 10.4161/cc.7.11.5977.
64. Shi, X.-B., Xue, L., Yang, J., Ma, A.-H., Zhao, J., Xu, M., et al. (2007). An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc. Natl. Acad. Sci. U.S.A. 104, 19983-19988. doi: 10.1073/pnas.0706641104.
65. Somasundaram, R., and Schuppan, D. (1996). Type I, II, III, IV, V, and VI collagens serve as extracellular ligands for the isoforms of platelet-derived growth factor (AA, BB, and AB). J. Biol. Chem. 271, 26884-26891. doi: 10.1074/jbc.271.43.26884.
66. Tinsley, J. M., Blake, D. J., Zuellig, R. A., and Davies, K. E. (1994). Increasing complexity of the dystrophin-associated protein complex. Proc. Natl. Acad. Sci. U.S.A. 91, 8307-8313. doi: 10.1073/pnas.91.18.8307.
67. Varghese, J., and Cohen, S. M. (2007). microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev. 21, 2277-2282. doi: 10.1101/gad.439807.
68. Varghese, J., Lim, S. F., and Cohen, S. M. (2010). Drosophila miR-14 regulates insulin production and metabolism through its target, sugarbabe. Genes Dev. 24, 2748-2753. doi: 10.1101/gad.1995910.
69. Villarreal, G., Oh, D.-J., Kang, M. H., and Rhee, D. J. (2011). Coordinated regulation of extracellular matrix synthesis by the microRNA-29 family in the trabecular meshwork. Invest. Ophthalmol. Vis. Sci. 52, 3391-3397. doi: 10.1167/iovs.10-6165.
70. Vo, N., Klein, M. E., Varlamova, O., Keller, D. M., Yamamoto, T., Goodman, R. H., et al. (2005). A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 16426-16431. doi: 10.1073/pnas.0508448102.
71. Wang, G., Mao, W., Zheng, S., and Ye, J. (2009). Epidermal growth factor receptor-regulated miR-125a-5p-a metastatic inhibitor of lung cancer. FEBS J. 276, 5571-5578. doi: 10.1111/j.1742-4658.2009.07238.x.
72. Wijelath, E. S., Rahman, S., Namekata, M., Murray, J., Nishimura, T., Mostafavi-Pour, Z., et al. (2006). Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain: enhancement of VEGF biological activity by a singular growth factor/matrix protein synergism. Circ. Res. 99, 853-860. doi: 10.1161/01.RES.0000246849.17887.66.
73. Williamson, R. A., Henry, M. D., Daniels, K. J., Hrstka, R. F., Lee, J. C., Sunada, Y., et al. (1997). Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6, 831-841. doi: 10.1093/hmg/6.6.831.
74. Xiong, Y., Zhou, Y., and Jarrett, H. W. (2009). Dystrophin glycoprotein complex-associated Gbetagamma subunits activate phosphatidylinositol-3-kinase/Akt signaling in skeletal muscle in a laminin-dependent manner. J. Cell. Physiol. 219, 402-414. doi: 10.1002/jcp.21684.
75. Yang, B., Jung, D., Motto, D., Meyer, J., Koretzky, G., and Campbell, K. P. (1995). SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem. 270, 11711-11714. doi: 10.1074/jbc.270.20.11711.
76. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M. (1991). Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848. doi: 10.1016/0092-8674(91)90512-W.
77. Yu, W. H., and Woessner, J. F. (2000). Heparan sulfate proteoglycans as extracellular docking molecules for matrilysin (matrix metalloproteinase 7). J. Biol. Chem. 275, 4183-4191. doi: 10.1074/jbc.275.6.4183 t.
78. Yu, W. H., Yu, S., Meng, Q., Brew, K., and Woessner, J. F. (2000). TIMP-3 binds to sulfated glycosaminoglycans of the extracellular matrix. J. Biol. Chem. 275, 31226-31232. doi: 10.1074/jbc.M000907200.
79. Zhang, X., Liu, S., Hu, T., Liu, S., He, Y., and Sun, S. (2009). Up-regulated microRNA-143 transcribed by nuclear factor kappa B enhances hepatocarcinoma metastasis by repressing fibronectin expression. Hepatology 50, 490-499. doi: 10.1002/hep.23008.
80. Zhou, Y. W., Thomason, D. B., Gullberg, D., and Jarrett, H. W. (2006). Binding of laminin alpha1-chain LG4-5 domain to alpha-dystroglycan causes tyrosine phosphorylation of syntrophin to initiate Rac1 signaling. Biochemistry 45, 2042-2052. doi: 10.1021/bi0519957.
81. Zhu, Y., Oganesian, A., Keene, D. R., and Sandell, L. J. (1999). Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta1 and BMP-2. J. Cell Biol. 144, 1069-1080. doi: 10.1083/jcb.144.5.1069.