Fucoidan reduces secretion and expression of vascular endothelial growth factor in the retinal pigment epithelium and reduces angiogenesis in vitro

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Dithmer, Michaela ^a   Fuchs, Sabine ^a   Shi, Yang ^a   Schmidt, Harald ^b   Richert, Elisabeth ^a   Roider, Johann ^a   Klettner, Alexa ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b University of Kiel University Medical Center Experimental Trauma Surgery ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; FUCOIDIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL PROLIFERATION; CHOROID; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; EXPLANT; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PHAGOCYTOSIS; PIGMENT CELL; PIGMENT EPITHELIUM; PROTEIN EXPRESSION; PROTEIN SECRETION; SWINE; WOUND HEALING;

ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE; COLLAGEN; DRUG COMBINATIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; LAMININ; MACULAR DEGENERATION; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PHYSIOLOGIC; POLYSACCHARIDES; PROTEOGLYCANS; RETINAL PIGMENT EPITHELIUM; TETRAZOLIUM SALTS; THIAZOLES; TRYPAN BLUE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84896754447     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089150     Document Type: Article

References (52)

1. Schrader WF (2006) Age-related macular degeneration: a socioeconomic time bomb in our aging society. Ophthalmologe 103: 742-748.
2. Zarbin M (2004) Current concepts in the pathogenesis of age-related macular degeneration. Arch Ophthalmol 122: 598-614.
3. Sparrow JR, Ueda K, Zhou J (2012) Complement dysregulation in AMD: RPE-Bruch's membrane-choroid. Mol Aspects Med 33: 436-445.
4. Parmeggiani F, Romano MR, Costagliola C, Semeraro F, Incorvaia C, et al. (2012) Mechanism of inflammation in age-related macular degeneration. Mediators Inflamm 2012: 546786.
5. Miller DW, Joussen AM, Holz FG (2003) The molecular mechanisms of age-related macular degeneration. Ophthalmologe 100: 92-96. (Pubitemid 36723500)
6. Lu M, Adamis AP (2006) Molecular biology of choroidal neovascularization. Ophthalmol Clin North Am 19: 323-334. (Pubitemid 44403942)
7. Miller JW, Le Couter J, Strauss EC, Ferrara N (2013) Vascular endothelial growth factor a in intraocular vascular disease. Ophthalmology 120: 106-114.
8. Rosenfeld PJ, Rich RM, Lalwani GA (2006) Ranibizumab: Phase III clinical trial results. Ophthalmol Clin North Am 19: 361-372. (Pubitemid 44279358)
9. Hodge W, Brown A, Kymes S, Cruess A, Blackhouse G, et al. (2010) Pharmacologic management of neovascular age-related macular degeneration: systematic review of economic evidence and primary economic evaluation. Can J Ophthalmol 45: 223-230.
10. Saint-Geniez M, Maldonado AE, D'Amore PA (2006) VEGF expression and receptor activation in the choroid during development and in the adult. Invest Ophthalmol Vis Sci 47: 3135-3142. (Pubitemid 351639793)
11. Blaauwgeers HGT, Holtkamp GM, Rutten H, Witmer AN, Koolwijk P, et al. (1999) Polarized vascular endothelial growth factor secretion by human retinal pigment epithelium and localization of vascular endothelial growth factor receptors on the inner choriocapillaris. Evidence for a trophic paracrine relation. Am J Pathol 155: 421-428. (Pubitemid 29370392)
12. Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85: 845-881.
13. Peters S, Heiduschka P, Julien S, Ziemssen F, Fietz H, et al. (2007) Ultrastructural findings in the primate eye after intravitreal injection of bevacizumab. Am J Ophthalmol 143: 995-1002.
14. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, et al. (1998) Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343. (Pubitemid 28545503)
15. Klettner A, Roider J (2012) Mechanisms of Pathological VEGF Production in the Retina and Modification with VEGF-Antagonists. In: Stratton R, Hauswirth W, Gardner T, editors. Oxidative Stress in Applied Basic Research and Clinical Practise: Studies on Retinal and Choroidal Disorders. Humana Press. pp. 277-307.
16. Campochiaro P, Soloway P, Ryan SJ, Miller JW (1999) The pathogenesis of choroidal neovascularization in patients with age-related macular degeneration. Mol Vis 5: 34-38.
17. Schlingemann RO (2004) The role of growth factors and the wound healing response in age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 242: 91-101.
18. Fitton JH (2011) Therapies from fucoidan; multifunctional marine polymers. Mar Drugs 9: 1731-1760.
19. Tissot B, Montdargent B, Chevolot L, Varenne A, Descroix S, et al. (2003) Interaction of fucoidan with the protein of the complement classical pathway. Biochim Biophys Acta 1651: 5-16. (Pubitemid 38234548)
20. Rocha de Souza MC, Marques CT, Guerra Dore CM, Ferreira da Silva FR, Oliveira Rocha HA, et al. (2007) Antioxidant activities of sulfated polysaccharides form brown and red seaweeds. J Appl Phycol 19: 153-160.
21. Cumashi A, Ushakova N, Preobrazhenskaya ME, D'Incecco A, Piccoli A, et al. (2007) A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of the nine different fucoidans from brown seaweed. Glycobiology 17: 541-552. (Pubitemid 47049941)
22. Azuma K, Ishihara T, Nakamoto H, Amaha T, Osaki T, et al. (2012) Effects of oral administration of fucoidan extracted from Cladosiphon okamuranus on tumor growth and survival time in a tumor bearing mouse model. Mar Drugs 10: 2337-2348.
23. Myers SP, O'Connor J, FittonJH, Brooks L, Rolfe M, et al. (2010) A combined phase I and phase II open label study on the effects of a seaweed extract nutrient complex on osteoarthritis. Biologics 4: 33-4-4.
24. Irhimeh MR, FittonJH, Lowenthal RM (2007) Fucoidan ingestion increases the expression of CXCR4 on human CD34+ cells. Exp Hematol 35: 989-994. (Pubitemid 46802979)
25. Li N, Zhang Q, Song J (2005) Toxicological evaluation of fucoidan extracted from Laminaria japonica in Wistar rats. Food Chem Toxicol 43: 421-426. (Pubitemid 40170474)
26. Abe S, Hiramatsu K, Ichikawa O, Kawamoto H, Kasagi T, et al. (2013) Safety evaluation of excessive ingestion of mozuku fucoidan in human. J Food Sci 78: T648-T651.
27. Koyanagi S, Tanigawa N, Nakagawa H, Soeda S, Shimeno H (2003) Oversulfation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem Pharmacol 65: 173-179. (Pubitemid 36015820)
28. Narazaki M, Segarra M, Tosato G (2008) Sulfated polysaccharides identified as inducers of neuropilin-1 internalization and functional inhibition of VEGF165 and semaphorin3A. Blood 111: 4126-4136.
29. Wiencke AK, Kiilgaard JF, Nicolini J, Bundgaard M, Ropke C, et al. (2003) Growth of cultured porcine retinal pigment epithelial cells. Acta Ophthalmol Scand 81: 170-176. (Pubitemid 36609220)
30. Klettner A, Roider J (2008) Comparison of bevacizumab, ranibizumab and pegaptanib in vitro: efficiency and possible additional pathways. Invest Ophthalmol Vis Sci 49: 4523-4527.
31. Miura Y, Klettner A, Noelle B, Hasselbach H, Roider J (2010) Change of morphological and functional characteristics of retinal pigment epithelium cells during cultivation of retinal pigment epithelium-choroid perfusion tissue culture. Ophthalmic Res 43: 122-133.
32. Minuth WW, Steiner P, Strehl R, Schumacher K, de Vries U, et al. (1999) Modulation of cell differentiation in perfusion culture. Exp Nephrol 7: 394-406. (Pubitemid 29517349)
33. Klettner A, Westhues D, Lassen J, Bartsch S, Roider J (2013) Regulation of constitutive vascular endothelial growth factor secretion in retinal pigment epithelium/choroid organ cultures: p38, nuclear factor κB, and the vascular endothelial growth factor receptor-2/phosphatidylinositol 3 kinase pathway. Mol Vis 19: 281-291.
34. Klettner AK, Kruse ML, Meyer T, Wesch D, Kabelitz D, et al (2009) Different properties of VEGF-antagonists: Bevacizumab but not Ranibizumab accumulates in RPE cells. Graefes Arch Clin Exp Ophthalmol 247: 1601-1608.
35. Klettner A, Koinzer S, Waetzig V, Herdegen T, Roider J (2010) Deferoxamine mesylate is toxic for retinal pigment epithelium cells, and its toxicity is mediated by p38. Gutan Ocul Toxicol 29:122-129.
36. Klettner A, Möhle F, Lucius R, Roider J (2011) Quantifying FITC-labeled latex beads opsonized with photoreceptor outer segment fragments: an easy and inexpensive method of investigating phagocytosis in retinal pigment epithelium cells. Ophthalmic Res 46: 88-91.
37. Fuchs S, Motta A, Migliaresi C, Kirkpatrick CJ (2006) Outgrowth endothelial cells isolated and expanded from human peripheral blood progenitor cells as a potential source of autologous cells for endothelialization of silk fibroin biomaterials. Biomaterials 27: 5399-5408. (Pubitemid 44093717)
38. Fuchs S, Hofmann A, Kirkpartrick C {2007) Microvessel-like structures from outgrowth endothelial cells from human peripheral blood in 2-dimensional and 3-dimensional co-cultures with osteoblastic lineage cells. Tissue Eng 13: 2577-2588. (Pubitemid 47571693)
39. Rasband WS (1997-2012) ImageJ, U. S. Nadonal Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/.
40. Fuchs S, Jiang X, Schmidt H, Dohle E, Ghanaati S, et al. (2009) Dynamic processes involved in the pre-vascularization of silk fibroin constructs for bone regeneration using outgrowth endothelial cells. Biomaterials 30: 1329-1338.
41. Cai H, Del Priore LV (2006) Gene expression profile of cultured adult compared to immortalized human RPE. Mol Vis 12:1-14. (Pubitemid 43046237)
42. Aisa Y, Miyakawa Y, Nakazato T, Shibata H, Saito K, et al. (2005) Fucoidan induces apoptosis of human HS-Sultan cells accompanied by activation of caspase-3 and down-regulation of ERK pathways. Am J Hematol 78: 7-14. (Pubitemid 40023740)
43. Kim EJ, Park SY, Lee JY, Park JH (2010) Fucoidan present in brown algae induces apoptosis of human colon cancer cells. BMC Gastroenterology 10: 96-107.
44. Riou D, Colliec-Jouault S, Pinczon du Sel D, Bosch S, Siavoshian S, et al. (1996) Antitumor and antiproliferative effects of a fucan extracted from ascophyllum nodosum against a non-small-cell bronchopulmonary carcinoma line. Anticancer Res 16: 1213-1218.
45. 4 integrin, and fucoidin receptor-mediated phagocytosis of apoptotic leukocytes. J Leukoc Biol 74: 810-820.
46. Liu JM, Bignon J, Haroun-Bouhedja F, Bittoun P, Vassy J, et al. (2005) Inhibitory effect of fucoidan on the adhesion of adenocarcinoma cells to fibronectin. Anticancer Res 25: 2129-2134.
47. Roider J, Michaud NA, Flotte TJ, Birngruber R (1992) Response of the retinal pigment epithelium to selective photocoagulation. Arch Ophthalmol 110: 1786-1792.
48. Caramoy A, Fauser S, Kirchhof B (2012) Fundus autofluorescence and spectral-domain optical coherence tomography findings suggesting tissue remodelling in retinal pigment epithelium tear. Br J Ophthalmol 96: 1211-1216.
49. Lopez PF, Yan Q, Kohen L, Rao NA, Spee C, et al. (1995) Retinal pigment epithelial wound healing in vivo. Arch Ophthalmol 113: 1437-1446.
50. Ho J, Witkin AJ, Liu J, Chen Y, Fujimoto JG, et al. (2011) Documentation of intraretinal retinal pigment epithelium migration via high-speed ultrahigh-resolution optical coherence tomography. Ophthalmology 118: 687-693.
51. Matou S, Helley D, Chabut D, Bros A, Fischer AM (2002) Effect of fucoidan on fibroblast growth factor-2-induced angiogenesis in vitro. Thromb Res 106: 213-221. (Pubitemid 35248054)
52. Araya N, Takahashi K, Sato T, Nakamura T, Sawa C, et al. (2011) Fucoidan therapy decreases the proviral load in patients with human T-lymphotropic virus type-1-associated neurological disease. Antivir Ther 16: 89-98.