S100a4 is upregulated in proliferative diabetic retinopathy and correlates with markers of angiogenesis and fibrogenesis

Molecular Vision

Volumn 20, Issue , 2014, Pages 1209-1224

  El Asrar, Ahmed M Abu ^a   Nawaz, Mohd Imtiaz ^a   Hertogh, Gert De ^b   Alam, Kaiser ^a   Siddiquei, Mohammad Mairaj ^a   Eynde, Kathleen Van Den ^b   Mousa, Ahmed ^a   Mohammad, Ghulam ^a   Geboes, Karel ^b   Opdenakker, Ghislain ^c  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CALVASCULIN; CD31 ANTIGEN; CD45 ANTIGEN; CYTOKINE; OSTEOPONTIN; SYNDECAN 1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; BIOLOGICAL MARKER; PROTEIN S 100; S100A4 PROTEIN, HUMAN; S100A4 PROTEIN, RAT; SDC1 PROTEIN, HUMAN; SPP1 PROTEIN, RAT; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE ACTIVITY; DISEASE COURSE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIRETINAL MEMBRANE; EXTRACELLULAR MATRIX; FIBROGENESIS; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; RETINA; RETINA DETACHMENT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; STROMA CELL; UPREGULATION; VITRECTOMY; VITREOUS BODY; WESTERN BLOTTING; ANIMAL; CASE CONTROL STUDY; CELL CULTURE; ENDOTHELIUM CELL; EXPERIMENTAL DIABETES MELLITUS; FIBROSIS; METABOLISM; PATHOLOGY; RETINA BLOOD VESSEL; RETINA NEOVASCULARIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; BIOMARKERS; CASE-CONTROL STUDIES; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOTHELIAL CELLS; FIBROSIS; HUMANS; MALE; OSTEOPONTIN; RATS; RATS, SPRAGUE-DAWLEY; RETINAL NEOVASCULARIZATION; RETINAL VESSELS; S100 PROTEINS; SYNDECAN-1; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VITREOUS BODY;

EID: 84908670753     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Joussen, AM, Poulaki, V, Le, ML, Koizumi, K, Esser, C, Janicki, H, Schraermeyer, U, Kociok, N, Fauser, S, Kirchhof, B, Kern, TS. Adamis, AP. A central role for inflammation in the patho-genesis of diabetic retinopathy. FASEB J 2004; 18:1450 [PMID: 15231732].
2. Kaji, Y, Usui, T, Ishida, S, Yamashiro, K, Moore, TC, Moore, J, Yamamoto, Y, Yamamoto, H, Adamis, AP. Inhibition of diabetic leukostasis and blood-retinal barrier breakdown with a soluble form of a receptor for advanced glycation end products. Invest Ophthalmol Vis Sci 2007; 48:858 [PMID: 172 514 8 8].
3. Kim, YW, West, XZ, Byzova, TV. Inflammation and oxidative stress in angiogenesis and vascular disease. J Mol Med (Berl) 2013; 91:323-8. [PMID: 23430240].
4. Ono, M. Molecular links between tumor angiogenesis and inflammation: inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci 2008; 99:1501-6. [PMID: 1875 4859].
5. Abu El-Asrar, AM, Nawaz, MI, Kangave, D, Siddiquei, MM, Geboes, K. Angiogenic and vasculogenic factors in the vitreous from patients with proliferative diabetic retinopathy. J Diabetes Res. 2013; 2013 [PMID: 23671874].
6. Abu El-Asrar, AM, Imtiaz Nawaz, M, Kangave, D, Siddique, MM, Geboes, K. Osteopontin and other regulators of angio-genesis and fibrogenesis in the vitreous from patients with proliferative vitreoretinal disorders. Mediators Inflamm 2012; 2012:493043 [PMID: 23055574].
7. El-Asrar, AM, Nawaz, MI, Kangave, D, Geboes, K, Ola, MS, Ahmad, S, Al-Shabrawey, M. High-mobility group box-1 biomarkers of inflammation in the vitreous from patients with proliferative diabetic retinopathy. Mol Vis 2011; 17:1829-38. [PMID: 21850157].
8. Nawaz, MI, Van Raemdonck, K, Mohammad, G, Kangave, D, Van Damme, J, Abu El-Asrar, AM, Struyf, S. Autocrine CCL2, CXCL4, CXCL9 and CXCL10 signal in retinal endothelial cells and are enhanced in diabetic retinopathy. Exp Eye Res 2013; 109:67-76. [PMID: 23352833].
9. Deryugina, EI, Quigley, JP. Pleiotropic roles of matrix metal-loproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions. Biochim Biophys Acta 2010; 1803:103-20. [PMID: 19800930].
10. Spranger, J, Pfeiffer, AF. New concepts in pathogenesis and treatment of diabetic retinopathy. Exp Clin Endocrinol Diabetes 2001; 109:Suppl 2, S438-50. [PMID: 114 6 059 0].
11. Abu El-Asrar, AM, Mohammad, G, Nawaz, MI, Siddique, MM, Van den Eynde, K, Mousa, A, De Hertogh, G, Opdenakker, G. Relationship between vitreous levels of matrix metallopro-teinases and vascular endothelial growth factor in prolifera-tive diabetic retinopathy. PLoS ONE 2013; 8:e85857 [PMID: 2 439 2 031].
12. Saleem, M, Kweon, MH, Johnson, JJ, Adhami, VM, Elcheva, I, Khan, N. Bin Hafeez, B. Bhat, KM, Sarfaraz, S. Reagan-Shaw, S, Spiegelman, VS, Setaluri, V, Mukhtar, H. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metallopro-teinase 9. Proc Natl Acad Sci USA 2006; 103:14825-30. [PMID: 1699 0 429].
13. Zhang, J, Zhang, DL, Jiao, XL, Dong, Q. S100A4 regulates migration and invasion in hepatocellular carcinoma HepG2 cells via NK-κB-dependent MMP-9 signal. Eur Rev Med Pharmacol Sci 2013; 17:2372-82. [PMID: 24065232].
14. Boye, K, Maelandsmo, GM. S100A4 and metastasis: a small actor playing many roles. Am J Pathol 2010; 176:528-35. [PMID: 20 01918 8].
15. de Silva Rudland, S, Martin, L, Roshanlall, C, Winstanley, J, Leinster, S, Platt-Higgins, A, Carroll, J, West, C, Barraclough, R, Rudland, P. Association of S100A4 and osteopontin with specific prognostic factors and survival of patients with minimally invasive breast cancer. Clin Cancer Res 2006; 12:1192-200. [PMID: 16 489 073].
16. Tamaki, Y, Iwanaga, Y, Niizuma, S, Kawashima, T, Kato, T, Inuzuka, Y, Horie, T, Morooka, H, Takase, T, Akahashi, Y, Kobuke, K, Ono, K, Shioi, T, Sheikh, SP, Ambartsumian, N, Lukanidin, E, Koshimizu, T, Miyazaki, S, Kimura, T. Metastasis-associated protein, S100A4 mediates cardiac fibrosis potentially through the modulation of p53 in cardiac fibro-blasts. J Mol Cell Cardiol 2013; 57:72-81. [PMID: 2 33529 91].
17. He, J, Xu, Y, Koya, D, Kanasaki, K. Role of the endothelial-to-mesenchymal transition in renal fibrosis of chronic kidney disease. Clin Exp Nephrol 2013; 17:488-97. [PMID: 23430 391].
18. Zeisberg, EM, Potenta, SE, Sugimoto, H, Zeisberg, M, Kalluri, R. Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J Am Soc Nephrol 2008; 19:2282-7. [PMID: 1898730 4].
19. Tang, RN, Lv, LL, Zhang, JD, Dai, HY, Li, Q, Zheng, M, Ni, J, Ma, KL, Liu, BC. Effects of angiotensin II receptor blocker on myocardial endothelial-to-mesenchymal transition in diabetic rats. Int J Cardiol 2013; 162:92-9. [PMID: 2170 4391].
20. Widyantoro, B, Emoto, N, Nakayama, K, Anggrahini, DW, Adiarto, S, Iwasa, N, Yagi, K, Miyagawa, K, Rikitake, Y, Suzuki, T, Kisanuki, YY, Yanagisawa, M, Hirata, K. Endo-thelial cell-derived endothelin-1 promotes cardiac fibrosis in diabetic hearts through stimulation of endothelial-to-mesenchymal transition. Circulation 2010; 121:2407-18. [PMID: 20497976].
21. Österreicher, CH, Penz-Österreicher, M, Grivennikov, SI, Guma, M, Koltsova, EK, Datz, C, Sasik, R, Hardiman, G, Karin, M, Brenner, DA. Fibroblast-specific protein 1 identified an inflammatory subpopulation of macrophages in the liver. Proc Natl Acad Sci USA 2011; 108:308-13. [PMID: 21173249].
22. Senolt, L, Grigorian, M, Lukanidin, E, Simmen, B, Michel, BA, Pavelka, K, Gay, RE, Gay, S, Neidhart, M. S100A4 is expressed at site of invasion in rheumatoid arthritis synovium and modulates production of matrix metalloproteinases. Ann Rheum Dis 2006; 65:1645-8. [PMID: 17105852].
23. Klingelhöfer, J, Senolt, L, Baslund, B, Nielsen, GH, Skibshøj, I, Pavelka, K, Neidhart, M, Gay, S, Ambartsumian, N, Hansen, BS, Petersen, J, Lukanidin, E, Grigorian, M. Up-regulation of metastasis-promoting S100A4 (Mts-1) in rheumatoid arthritis: putative involvement in the pathogenesis of rheumatoid arthritis. Arthritis Rheum 2007; 56:779-789 [PMID: 17328 0 50].
24. Oslejsková, L, Grigorian, M, Gay, S, Neidhart, M, Senolt, L. The metastasis associated protein S100A4: a potential novel link to inflammation and consequent aggressive behavior of rheumatoid arthritis synovial fibroblasts. Ann Rheum Dis 2008; 67:1499-504. [PMID: 18 056757].
25. Schneider, M, Hansen, J, Sheikh, SP. S100A4: a common mediator of epithelial-mesenchymal transition, fibrosis and regeneration in diseases? J Mol Med (Berl) 2008; 86:507-22. [PMID: 1832 2670].
26. Helfman, DM, Kim, EJ, Lukanidin, E, Grigorian, M. The metastasis associated protein S100A4: role in tumour progression and metastasis. Br J Cancer 2005; 92:1955-8. [PMID: 15900299].
27. Jia, W, Gao, XJ, Zhang, ZD, Yang, ZX, Zhang, G. S100A4 silencing suppresses proliferation, angiogenesis and invasion of thyroid cancer cells through downregulation of MMP-9 and VEGF. Eur Rev Med Pharmacol Sci 2013; 17:1495-508. [PMID: 23771538].
28. O’Connell, JT, Sugimoto, H, Cooke, VG, MacDonald, BA, Mehta, AI, LeBleu, VS, Dewar, R, Rocha, RM, Brentani, RR, Resnick, MB, Neilson, EG, Zeisberg, M, Kalluri, R. VEGF-A and Tenascin-C produced by S100A4+ stromal cells are important for metastatic colonization. Proc Natl Acad Sci USA 2011; 108:16002-7. [PMID: 21911 39 2].
29. Kelly, DJ, Chanty, A, Gow, RM, Zhang, Y, Gilbert, RE. Protein kinase CB inhibition attenuates osteopontin expression, macrophage recruitment, and tubulointerstitial injury in advanced experimental diabetic nephropathy. J Am Soc Nephrol 2005; 16:1654-60. [PMID: 15843473].
30. Naldini, A, Leali, D, Pucci, A, Morena, E, Carraro, F, Nico, B, Ribatti, D, Presta, M. Cutting edge: IL-1 β mediates the proan-giogenic activity of osteopontin-activated human monocytes. J Immunol 2006; 177:4267-70. [PMID: 16982859].
31. Kohan, M, Breuer, R, Berkman, N. Osteopontin induces airway remodeling and lung fibroblast activation in a murine model of asthma. Am J Respir Cell Mol Biol 2009; 41:290-6. [PMID: 19151319].
32. Pardo, A, Gibson, K, Cisneros, J, Richards, TJ, Yang, Y, Becerril, C, Yousem, S, Herrera, I, Ruiz, V, Selman, M, Kaminski, N. Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med 2005; 2:e251 [PMID: 16128620].
33. Lenga, Y, Koh, A, Perera, AS, McCulloch, CA, Sodek, J, Zohar, R. Osteopontin expression is required for myofibroblast differentiation. Circ Res 2008; 102:319-27. [PMID: 18079410].
34. Sabo-Attwood, T, Ramos-Nino, ME, Eugenia-Ariza, M, MacPherson, MB, Butnor, KJ, Vacek, PC, McGee, SP, Clark, JC, Steele, C, Mossman, BT. Osteopontin modulates inflammation, mucin production, and gene expression signatures after inhalation of asbestos in a murine model of fibrosis. Am J Pathol 2011; 178:1975-85. [PMID: 21514415].
35. Dai, J, Peng, L, Fan, K, Wang, H, Wei, R, Ji, G, Cai, J, Lu, B, Li, B, Zhang, D, Kang, Y, Tan, M, Qian, W, Guo, Y. Osteopontin induces angiogenesis through activation of PI3K/AKT and ERK1/2 in endothelial cells. Oncogene 2009; 28:3412-22. [PMID: 19597469].
36. 3 integrin reduces tumor growth of human lung cancer cells in mice. Lung Cancer 2007; 57:302-10. [PMID: 174 8 2 311].
37. Du, XL, Jiang, T, Sheng, XG, Gao, R, Li, QS. Inhibition of osteo-pontin suppresses in vitro and in vivo angiogenesis in endo-metrial cancer. Gynecol Oncol 2009; 115:371-6. [PMID: 19783287].
38. Wang, Y, Yan, W, Lu, X, Qian, C, Zhang, J, Li, P, Shi, L, Zhao, P, Fu, Z, Pu, P, Kang, C, Jiang, T, Liu, N, You, Y. Overexpression of osteopontin induces angiogenesis of endothelial progenitor cells via the αvβ3/PI3K/AKT/eNOS/NO signaling pathway in glioma cells. Eur J Cell Biol 2011; 90:642-8. [PMID: 21616 556].
39. Denhardt, DT, Noda, M, O’Regan, AW, Pavlin, D, Berman, JS. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 2001; 107:1055-61. [PMID: 113 42 56 6].
40. Huang, Q, Sheibani, N. High glucose promotes retinal endothelial migration through activation of Src, PI3K/Akt1/eNOS, and ERKs. Am J Physiol Cell Physiol 2008; 295:C1647-57. [PMID: 18945941].
41. Takemoto, M, Yokotc, K, Nishimura, M, Shigematsu, T, Hasegawa, T, Kon, S, Uede, T, Matsumoto, T, Saito, Y, Mori, S. Enhanced expression of osteopontin in human diabetic artery and analysis of its functional role in accelerated athero-genesis. Arterioscler Thromb Vasc Biol 2000; 20:624-8. [PMID: 10712383].
42. Junaid, A, Amara, FM. Osteopontin: correlation with interstitial fibrosis in human diabetic kidney and PI3-kinase-mediated enhancement of expression by glucose in human proximal tubular epithelial cells. Histopathology 2004; 44:136-46. [PMID: 1476 4 057].
43. Chakraborty, G, Jain, S, Kundu, GC. Osteopontin promotes vascular endothelial growth factor-dependent breast tumor growth and angiogenesis via autocrine and paracrine mechanisms. Cancer Res 2008; 68:152-61. [PMID: 1817230 7].
44. Berge, G, Pettersen, S, Grotterød, I, Bettum, IJ, Boye, K, Mælandsmo, GM. Osteopontin—an important downstream effector of S100A4-mediated invasion and metastasis. Int J Cancer 2011; 129:780-90. [PMID: 20 957651].
45. Teng, YH, Aquino, RS, Park, PW. Molecular functions of syndecan-1 in disease. Matrix Biol 2012; 31:3-16. [PMID: 22033227].
46. Manon-Jensen, T, Multhaupt, HAB, Couchman, JR. Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains. FEBS J 2013; 280:2320-31. [PMID: 2 338 4311].
47. Aiello, LP, Avery, RL, Arrig, PG, Keyt, BA, Jampel, HD, Shah, ST, Pasquale, LR, Thieme, H, Iwamoto, MA, Park, JE, Nguyen, H V, Aiello, LM, Ferrara, N, King, GL. Vascular endothelial growth factor in ocular fluid in patients with diabetic reti-nopathy and other retinal disorders. N Engl J Med 1994; 331:1480-7. [PMID: 7526212].
48. Bishop, PN. Structural macromolecules and supramolecular organization of the vitreous gel. Prog Retin Eye Res 2000; 19:323-44. [PMID: 10749380].
49. Sebag, J. Anomalous posterior vitreous detachment: a unifying concept in vitreo-retinal disease. Graefes Arch Clin Exp Ophthalmol 2004; 242:690-8. [PMID: 15309558].
50. van Deemter, M, Pas, HH, Kuijer, R, van der Worp, RJ, Hooymans, JM, Los, LI. Enzymatic breakdown of type II collagen in the human vitreous. Invest Ophthalmol Vis Sci 2009; 50:4552-60. [PMID: 19420340].
51. Abu El-Asrar, AM, Missotten, L, Geboes, K. Expression of advanced glycation end products and related molecules in diabetic fibrovascular epiretinal membranes. Clin Experiment Ophthalmol 2010; 38:57-64. [PMID: 20447102].
52. Le Hir, M, Hegyi, I, Cueni-Loffing, D, Loffing, J, Kaissling, B. Characterization of renal interstitial fibroblast-specific protein 1/S100A4-positive cells in healthy and inflamed rodent kidneys. Histochem Cell Biol 2005; 123:335-46. [PMID: 15856273].
53. Ambartsumian, N, Klingelhöfer, J, Grigorian, M, Christensen, C, Kriajevska, M, Tulchinsky, E, Georgiev, G, Berezin, V, Bock, E, Rygaard, J, Cao, R, Cao, Y, Lukanidin, E. The metastasis-associated Mts1 (S100A4) protein could act as an angiogenic factor. Oncogene 2001; 20:4685-95. [PMID: 11498791].
54. Hernández, JL, Padilla, L, Dakhel, S, Coll, T, Hervas, R, Adan, J, Masa, M, Mitjans, F, Martinez, JM, Coma, S, Rodríguez, L, Noé, V, Ciudad, CJ, Blasco, F, Messeguer, R. Therapeutic targeting of tumor growth and angiogenesis with a novel anti-S100A4 monoclonal antibody. PLoS ONE 2013; 8:e72480 [PMID: 24023743].
55. Ochiya, T, Takenaga, K, Endo, H. Silencing of S100A4, a metastasis-associated protein, in endothelial cells inhibits tumor angiogenesis and growth. Angiogenesis 2014; 17:17-26. [PMID: 23929008].
56. Yang, H, Zhao, K, Yu, Q, Wang, X, Song, Y, Li, R. Evaluation of plasma and tissue S100A4 protein and mRNA levels as potential markers of metastasis and prognosis in clear cell renal cell carcinoma. J Int Med Res 2012; 40:475-85. [PMID: 22613408].
57. Ai, KX, Lu, LY, Huang, XY, Chen, W, Zhang, HZ. Prognostic significance of S100A4 and vascular endothelial growth factor expression in pancreatic cancer. World J Gastroenterol 2008; 14:1931-5. [PMID: 18350635].
58. Dahlmann, M, Okhrimenko, A, Marcinkowski, P, Osterland, M, Herrmann, P, Smith, J, Heizmann, CW, Schlag, PM, Stein, U. RAGE mediates S100 A4-induced cell motility via MAPK/ ERK and hypoxia signaling and is a prognostic biomarker for human colorectal cancer metastasis. Oncotarget 2014; 5:3220-33. [PMID: 24952599].
59. Mohammad, G, Siddique, MM, Othman, A, Al-Shabrawey, M, Abu El-Asrar, AM. High-mobility group box-1 protein activates inflammatory signaling pathway components and disrupts retinal vascular-barrier in diabetic retina. Exp Eye Res 2013; 107:101-9. [PMID: 23261684].
60. El-Asrar, AM, Missotten, L, Geboes, K. Expression of high-mobility groups box-1/receptor for advanced glycation end products/osteopontin/early growth response-1 pathway in proliferative vitreoretinal epiretinal membranes. Mol Vis 2011; 17:508-18. [PMID: 21365018].
61. Agnihotri, R, Crawford, HC, Haro, H, Matrisian, LM, Havrda, MC, Liaw, L. Osteopontin, a novel substrate for matrix metalloproteinase-3 (Stromelysin-1) and matrix metallo-proteinase-7 (Matrilysin). J Biol Chem 2001; 276:28261-7. [PMID: 113759 93].
62. Takafuji, V, Forgues, M, Unsworth, E, Goldsmith, P, Wang, XW. An osteopontin fragment is essential for tumor cell invasion in hepatocellular carcinoma. Oncogene 2007; 26:6361-71. [PMID: 17452979].
63. Tan, TK, Zheng, G, Hsu, T, Lee, SR, Zhang, J, Zhao, Y, Tian, X, Wang, Y, Wang, YM, Cao, Q, Wang, Y, Lee, VWS, Wang, C, Zheng, D, Alexander, SI, Thompson, E, Harris, DCH. Matrix metalloproteinase-9 of tubular and macrophage origin contributes to the pathogenesis of renal fibrosis via macro-phage recruitment through osteopontin cleavage. Lab Invest 2013; 93:434-49. [PMID: 23358111].
64. Gao, YA, Agnihotri, R, Vary, CPH, Liaw, L. Expression and characterization of recombinant osteopontin peptides representing matrix metalloproteinase proteolytic fragments. Matrix Biol 2004; 23:457-66. [PMID: 15579312].
65. Purushothaman, A, Uyama, T, Kobayashi, F, Yamada, S, Sugahara, K, Rapraeger, AC, Sanderson, RD. Heparanase-enhanced shedding of syndecan-1 by myeloma cells promotes endo-thelial invasion and angiogenesis. Blood 2010; 115:2449-57. [PMID: 20097882].
66. Yang, Y, MacLeod, V, Miao, H, Theus, A, Zhan, F, Shaughnessy, JD Jr, Sawyer, J, Li, J, Zcharia, E, Vlodavsly, I, Sanderson, RD. Haparanase enhances syndecan-1 shedding. A novel mechanism for stimulation of tumor growth and metastasis. J Biol Chem 2007; 282:13326-33. [PMID: 173 47152].