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Ocular neovascularization: a valuable model system

Oncogene volume 22, pages 6537–6548 (2003)Cite this article

Abstract

There is no unique formula for angiogenesis. Instead there is a large group of potential participating proteins that interact in complex ways. Depending upon the surrounding cell types and the relative expression levels of angiogenesis-related proteins, the ‘angiogenesis cascade’ can vary. Therefore, it is valuable to study and compare the role of proteins in several well-characterized vascular beds. The eye provides a useful model system, because it contains several vascular beds sandwiched between avascular tissue. This allows for unequivocal identification and quantitation of new vessels. Retina-specific promoters combined with inducible promoter systems provide a means to regulate the expression of proteins of interest. As a relatively isolated compartment, the eye also provides advantages for gene transfer. By gaining insight regarding the molecular signals involved in various types of ocular angiogenesis, general concepts can emerge that may apply to other settings, including tumor angiogenesis. One concept that has emerged is that despite participation of multiple stimulatory factors for ocular neovascularization, VEGF plays an essential role and interruption of VEGF signaling is an important therapeutic strategy. Another concept is that while most studies have focused on prevention of ocular neovascularization, regression of new vessels is desirable and is achievable with at least three agents, combretastatin A-4 phosphate, pigment epithelium-derived factor, and angiopoietin-2. Finally, endostatin and angiostatin, which have been sources of controversy because of inconsistent results in tumor models, have been shown to have good efficacy when delivered by gene transfer in models of ocular neovascularization. These results provide leads for new ocular treatments and perspective for evaluation of studies of neovascularization in extraocular tissues.

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References

  • Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, Wilks AF, Alitalo K and Stacker SA . (1998). Proc. Natl. Acad. Sci. USA, 95, 548–553.

  • Adamis AP, Shima DT, Tolentino MJ, Gragoudas ES, Ferrara N, Folkman J, D'Amore PA and Miller JW . (1996). Arch. Ophthalmol., 114, 66–71.

  • Aiello LP, Pierce EA, Foley ED, Takagi H, Chen H, Riddle L, Ferrara N, King GL and Smith LEH . (1995). Proc. Natl. Acad. Sci. USA, 92, 10457–10461.

  • Alon T, Hemo I, Itin A, Pe'er J, Stone J and Keshet E . (1995). Nat. Med., 1, 1024–1028.

  • Ando A, Mori K, Yamada H, Yamada E, Takahashi K, Saikia J, Yang A, Kim M and Campochiaro PA . (2001). J. Cell. Physiol., 191, 116–124.

  • Ando A, Yang A, Nambu H and Campochiaro PA . (2002). Mol. Pharmacol., 62, 539–544.

  • Beck H, Acker T, Wiessner C, Allegrini PR and Plate KH . (2000). Am. J. Pathol., 157, 1473–1483.

  • Brooks P, Clark R and Cheresh D . (1994a). Science, 264, 569–571.

  • Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, Klier G and Cheresh D . (1994b). Cell, 79, 1157–1164.

  • Brown LF, Berse B, Jackman RW, Tognazzi K, Manseau EJ, Dvorak JF and Senger DR . (1993). Am. J. Pathol., 143, 1255–1262.

  • Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewechin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D and Persico MG . (2001). Nat. Med., 7, 575–583.

  • Carmeliet P, Ng Y-S, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, Perriard J-C, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, Collen D, D'Amore PA and Shima DT . (1999). Nat. Med., 5, 495–502.

  • Chaplin DJ, Pettit GR and Hill SA . (1999). Anticancer Res, 19, 189–196.

  • Dark GD, Hill SA, Prise VE, Tozer GM, Pettit GR and Chaplin DJ . (1997). Cancer Res, 57, 1829–1834.

  • Das A, McLamore A, Song W and McGuire PO . (1999). Arch. Ophthalmol., 117, 498–503.

  • Davel LE, Miguez MM and de Lustig ES . (1985). Transplantation, 39, 564–565.

  • Davis S, Aldrich TH, Jones P, Acheson A, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC and Yancopoulos GD . (1996). Cell, 87, 1161–1169.

  • Dawson DW, Volpert OV, Gillis P, Crawford SE, Xu H-J, Benedict W and Bouck NP . (1999). Science, 285, 245–248.

  • Deutsch TA and Hughes WF . (1979). Am. J. Ophthalmol., 87, 536–540.

  • Diaz-Flores L, Gutierrez R, Valladares F, Varela H and Perez M . (1994). Anat. Rec., 238, 68–76.

  • Dowlati A, Robertson K, Cooney M, Petros WP, Stratford M, Jesberger J, Rafie N, Overnoyer B, Makkar V, Stambler B, Taylor A, Waas J, Lewin JS, McCrae KR and Remick SC . (2002). Cancer Res, 62, 3408–3416.

  • Dumont DJ, Gradwohl G, Fong G-H, Puri MC, Gerstenstein M, Auerbach A and Breitman ML . (1994). Genes Dev, 8, 1897–1909.

  • Edgren M., Lennernas B, Larrsson A and Nilsson S . (1999). Anticancer Res, 19, 869–873.

  • EyeTech Study Group (2002). Retina, 22, 143–152.

  • Form DM and Auerbach R . (1982). Proc. Soc. Exp. Biol. Med., 172, 214–218.

  • Friedlander M, Theesfeld CL, Sugita M, Fruttiger M, Thomas MA, Chang S and Cheresh DA . (1996). Proc. Natl. Acad. Sci. USA, 93, 9764–9769.

  • Gehlbach P, Demetriades AM, Yamamoto S, Deering T, Duh EJ, Yang HS, Cingolani C, Lai H, Wei L and Campochiaro PA . (2003a). Gene Therapy, 10, 637–646.

  • Gehlbach P, Demetriades AM, Yamamoto S, Deering T, Xiao WH, Duh EJ, Yang HS, Lai H, Kovesdi I, Wei L and Campochiaro PA . (2003b). Hum. Gene Ther., 14, 129–141.

  • Good DJ, Polverini PJ and Rastinejad F . et al. (1990). Proc. Natl. Acad. Sci. USA, 87, 6624–6628.

  • Gossen M, Freundlieb S, Bender G, Muller G, Hillen W and Bujard H . (1995). Science, 268, 1766–1769.

  • Grosios K, Holwell SE, McGown AT, Pettit GR and Bibby MC . (1999). Br. J. Canc., 81, 1318–1327.

  • Macular Photocoagulation Study Group (1991). Arch. Ophthalmol., 109, 1109–1114.

  • Gutheil JC, Campbell TN, Pierce PR, Watkins JD, Huse WD, Bodkin DJ and Cheresh DA . (2000). Clin. Cancer Res., 6, 3056–3061.

  • Hammes H, Brownlee M, Jonczyk A, Sutter A and Preissner K . (1996). Nat. Med., 2, 529–533.

  • Hangai M, Moon YS, Kitaya N, Chan CK, Wu D-Y, Peters KG, Ryan SJ and Hinton DR . (2001). Hum. Gene Ther., 12, 1311–1321.

  • Hayes AJ, Huang WQ, Mallah J, Yang D, Lippman ME and Li LY . (1999). Microvasc Res., 58, 224–237.

  • Hazzard TM, Christenson LK and Stouffer RL . (2000). Mol. Hum. Reprod., 6, 993–998.

  • Hill SA, Sonergan SJ, Denekamp J and Chaplin DJ . (1993). Eur. J. Cancer, 29A, 1320–1324.

  • Honda M, Sakamoto T, Ishibashi T, Inomata H and Ueno H . (2000). Gene Therapy, 7, 978–985.

  • Horsman M, Ehrnrooth E, Ladekarl M and Overgaard J . (1998). Int. J. Radial. Oncol. Biol. Phys., 42, 895–898.

  • Hynes RO . (2002). Nat. Med., 8, 918–921.

  • Janzer RC and Raff MC . (1987). Nature, 325, 253–257.

  • Jones MK, Wang H, Peskar BM, Levin E, Itani RM, Sarfeh IJ and Tarnawski AS . (1999). Nat. Med., 5, 1418–1423.

  • Joukov V, Pajusola K, Kaipainen K, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N and Alitalo K . (1996). EMBO J, 15, 290–298.

  • Kawamori T, Rao CV, Seibert K and Reddy BS . (1998). Cancer Res, 58, 409–412.

  • Kim I, Kim HG, Moon SO, Chae SW, So JN, Koh KN, Ahn BC and Koh GY . (2000a). Circ. Res., 86, 952–959.

  • Kim I, Kim HG, So J-N, Kim JH, Kwak HJ and Koh GY . (2000b). Circ. Res., 86, 24–29.

  • Klein R, Klein BEK, Moss SE, Davis MD and DeMets DL . (1984). Arch. Ophthalmol., 102, 520–526.

  • Koblizek TI, Weiss C, Yancopoulos GD, Deutsch U and Risau W . (1998). Curr. Biol., 8, 529–532.

  • Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, Joukov V and Alitalo K . (1996). Development, 122, 3829–3837.

  • Kwak HJ, So J-H, Lee SJ, Kim I and Koh GY . (1999). FEBS Lett, 448, 249–253.

  • Kwak N, Okamoto N, Wood JM and Campochiaro PA . (2000). Onvest. Ophthalmol. Vis. Sci., 41, 3158–3164.

  • Lai C-C, Wu W-C, Chen S-L, Xiao X, Tsai T-C, Huan S-J, Chen T-L, Tsai RJ-F and Tsao Y-P . (2001a). Invest. Ophthalmol. Vis. Sci., 42, 2401–2407.

  • Lai C-M, Brankov M, Zaknich T, Lai YK-Y, Shen W-Y, Constable IJ, Kovesdi I and Rakoczy PE . (2001b). Hum. Gene Ther., 12, 1299–1310.

  • Lambert V, Munaut C, Jost M, Noel A, Werb Z, Foidart JM and Rakic J-M . (2002). Am. J. Pathol., 161, 1247–1253.

  • Lambert V, Munaut C, Noel A, Frankenne F, Bajou K, Gerard R, Carmeliet P, Defresne MP, Foidart J-M and Rakic J-M . (2001). FASEB J, 15, 1021–1027.

  • Lee J, Gray A, Yuan J, Luoh SM, Avraham H and Wood WI . (1996). Proc. Patil. Acad. Sci. USA, 93, 1988–1992.

  • Lindahl P, Johansson BR, Leveen P and Betsholtz C . (1997). Science, 277, 242–245.

  • Luna J, Tobe T, Mousa SA, Reilly TM and Campochiaro PA . (1996). Lab. Invest., 75, 563–573.

  • Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ and Carmeliet PA . (2002). Nat. Med., 8, 831–839.

  • Maglione D, Guerriero V, Viglietto G, Delli-Bovi P and Persico MG . (1991). Proc. Natl. Acad. Sci. USA, 88, 9267–9271.

  • Maione TE, Gray GS, Petro J, Hunt AJ, Donner AL, Bauer SI, Carson HF and Sharpe RJ . (1990). Science, 247, 77–79.

  • Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN and Yancopoulos GD . (1997). Science, 277, 55–60.

  • Masferrer JL, Leahy KM, Koki AT, Zweifel BS, Settle SL, Woerner BM, Edwards DA, Flickinger AG, Moore RJ and Seibert K . (2000). Cancer Res, 60, 1306–1311.

  • Meyer M, Causs M, Lepple-Wienhues A, Waltengerger J, Augustin HG, Ziche M, Lanz C, Buttner M, Rziha H-J and Dehio C . (1999). EMBO J, 18, 363–374.

  • Miller H, Miller B and Ryan SJ . (1986). Invest. Ophthalmol. Vis. Sci., 27, 1644–1652.

  • Mordenti J, Cuthbertson RA, Ferrara N, Thomsen K, Berleau LT, Licko V, Allen PC, Valverde CR, Meng YG, Fei DT, Fourre KM and Ryan AM . (1999). Toxicol. Pathol., 27, 536–544.

  • Mori K, Ando A, Gehlbach P, Nesbitt D, Takahashi K, Goldsteen D, Penn M, Chen T, Mori K, Melia M, Phipps S, Moffat D, Brazzell K, Liau G, Dixon KH and Campochiaro PA . (2001a). Am. J. Pathol., 159, 313–320.

  • Mori K, Duh E, Gehlbach P, Ando A, Takahashi K, Pearlman J, Mori K, Yang HS, Zack DJ, Ettyreddy D, Brough DE, Wei LL and Campochiaro PA . (2001b). J. Cell. Physiol., 188, 253–263.

  • Mori K, Gehlbach P, Ando A, McVey D, Wei L and Campochiaro PA . (2001c). Invest. Ophthalmol. Vis. Sci., 43, 2428–2434.

  • Mori K, Gehlbach P, Yamamoto S, Duh E, Zack DJ, Li Q, Berns KI, Raisler BJ, Hauswirth WW and Campochiaro PA . (2002). Invest. Ophthalmol. Vis. Sci., 43, 1994–2000.

  • Nambu H, Nambu R, Melia M and Campochiaro PA . (2003). Invest. Ophthalmol. Vis. Sci. (in press).

  • Nicol D, Hii SI, Walsh M, Teh B, Thompson L, Kennett C and Gotley D . (1997). J. Urol., 157, 1482–1486.

  • Ohno-Matsui K, Hirose A, Yamamoto S, Saikia J, Okamoto N, Gehlbach P, Duh EJ, Hackett SF, Chang M, Bok D, Zack DJ and Campochiaro PA . (2002). Am. J. Pathol., 160, 711–719.

  • Okamoto N, Tobe T, Hackett SF, Ozaki H, Vinores MA, LaRochelle W, Zack DJ and Campochiaro PA . (1997). Am. J. Pathol., 151, 281–291.

  • Olofsson B, Pajusola K, Kaipainen A, Von Euler G, Joukov V, Saksel O, Orpana A, Pettersson RF, Alitalo K and Eriksson U . (1995). Proc. Natil. Acad. Sci. USA, 93, 2576–2581.

  • O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birknead JR, Olsen BR and Folkman J . (1997). Cell, 88, 277–285.

  • O'Reilly MS, Holmgren S, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage HE and Folkman J . (1994). Cell, 79, 315–328.

  • O'Reilly MS, Pirie-Sheherd S, Lane WS and Folkman J . (1999). Science, 285, 1926–1928.

  • Oshima Y, Oshima S, Takahashi K, Nambu H, Apte RS, Duh E, Hackett SF, Okoye G, Melia M, Wiegard S, Yancopoulos G, Zack DJ and Campochiaro PA . (2003). Different effects of angiopoietin 2 in different vascular beds; new vessels are most sensitive. Manuscript submitted.

  • Ozaki H, Hayashi H, Vinores SA, Moromizato Y, Campochiaro PA and Oshima K . (1997). Exp. Eye Res., 64, 505–517.

  • Ozaki H, Okamoto N, Ortega S, Chang M, Ozaki K, Sadda S, Vinores MA, Derevjanik N, Zack DJ, Basilico C and Campochiaro PA . (1998). Am. J. Pathol., 153, 757–765.

  • Ozaki H, Seo M-S, Ozaki K, Yamada H, Yamada E, Hofmann F, Wood J and Campochiaro PA . (2000). Am. J. Pathol., 156, 679–707.

  • Papapetropoulos A, Garcia-Cardena G, Dengler TJ, Maisonpierre PC, Yancopoulos GD and Sessa WC . (1999). Lab. Invest., 79, 213–223.

  • Park JE, Keller G-A and Ferrara N . (1993). Mol. Biol. Cell, 4, 1317–1326.

  • Pettit GR, Singh SB, Hamel E, Lin CM, Alberts DS and Garia-Kendall D . (1989). Experientia, 45, 205–211.

  • Pettit GR, Temple C, Narayanan VL, Varma R, Simpson MJ, Boyd MR, Rener GA and Banasal N . (1995). Anti-Cancer Drug Des, 10, 299–309.

  • Pichiule P and LaManna JC . (2002). J. Appl. Physiol., 93, 1131–1139.

  • Plate KH, Breier G, Welch HA and Risau W . (1992). Nature, 359, 845–848.

  • Posey JA, Khazaeli MB, DelGrosso A, Saleh MN, Lin CY, Huse WD and LoBuglio AF . (2001). Canc. Biother. Radiopharm., 16, 125–132.

  • Procopio WN, Pelavin PI, Lee WM and Yeilding NM . (1999). J. Biol. Chem., 274, 30196–30201.

  • Puri MC, Rossant J, Alitalo K, Bernstein A and Partanen J . (1995). EMBO J., 14, 5884–5891.

  • Raisler BJ, Berns KI, Grant MB, Beliaev D and Hauswirth WW . (2002). Proc. Natl. Acad. Sci. USA, 99, 8909–8914.

  • Rasmussen HS, Chu KW, Campochiaro P, Gehlbach P, Haller JA, Handa JT, Nguyen QD and Sung JU . (2001). Hum. Gene Ther., 12, 2029–2032.

  • Reichelt M, Shi S, Hayes M, Kay G, Batch J, Gole GA and Browning J . (2003). Clin. Exp. Ophthalmol., 31, 61–65.

  • Saishin Y, Saishin Y, Takahashi K, Lima Silva R, Hylton D, Rudge JS, Wiegard SJ and Campochiaro PA . (2003). J. Cell. Physiol., 195, 241–248.

  • Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, Gridley T, Wolburg H, Risau W and Qin Y . (1995). Nature, 376, 70–74.

  • Sawaoka H, Tsujii S, Tsujii M, Gunawan ES, Sasaki Y, Kawano S and Hori M . (1999). Lab. Invest., 79, 1469–1477.

  • Schwartz SD, Blumenkranz M, Rosenfeld PJ, Miller JW, Haller J, Fish G, Lobes L, Singerman L, Green WL and Reimann J . (2001). Invest. Ophthalmol. Vis. Sci., 42, Suppl S522.

  • Seed S, Slaughter DP and Limarzi LR . (1940). Surgery, 7, 696–709.

  • Seo M-S, Kwak N, Ozaki H, Yamada H, Okamoto N, Fabbro D, Hofmann F, Wood JM and Campochiaro PA . (1999). Am. J. Pathol., 154, 1743–1753.

  • Shweiki D, Itin A, Soffer D and Keshet E . (1992). Nature, 359, 843–845.

  • Smalley W and DuBois RN . (1997). Adv. Pharmacol., 39, 1–20.

  • Smith LEH, Kopchick JJ, Chen W, Knapp J, Kinose F, Daley D, Foley E, Smith RG and Schaeffer JM . (1997). Science, 276, 1706–1709.

  • Smith LEH, Wesolowski E, McLellan A, Kostyk SK, D'Amato R, Sullivan R and D'Amore PA . (1994). Invest. Ophthalmol. Vis. Sci., 35, 101–111.

  • Stalmans I, Ng Y-S, Rohan R, Fruttiger M, Bouche A, Yuce A, Fujisawa H, Hermans B, Sahni M, Jansen S, Hicklin D, Anderson DJ, Gardiner T, Hammes H-P, Moons L, Dewerchin M, Collen D, Carmeliet P and D'Amore PA . (2002). J. Clin. Invest., 109, 327–336.

  • Steele FR, Chader GJ, Johnson LV and Tombran-Tink J . (1993). Proc. Natl. Acad. Sci. USA, 90, 1526–1530.

  • Stone J, Itin A, Alon T, Pe'er J, Gnessin H, Chan-Ling T and Keshet E . (1995). J. Neurosci., 15, 4738–4747.

  • Suri C, Jones PP, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN and Yancopoulos GD . (1996). Cell, 87, 1171–1180.

  • Suri C, McClain J, Thurston G, McDonald DM, Zhou H, Oldmixon EH, Sato TN and Yancopoulos GD . (1998). Science, 282, 468–471.

  • Takahashi A, Sasaki H, Kim SJ, Tobisu D, Kakizoe T, Tsukamoto T, Kumamoto Y, Sugimura T and Terada M . (1994). Cancer Res, 54, 4233–4237.

  • Takahashi K, Saishin Y, Saishin Y, Lima Silva R, Oshima Y, Oshima S, Melia M, Paszkiet B, Zerby D, Kadan MJ, Liau G, Kaleko M, Connelly S, Luo T and Campochiaro PA . (2003a). FASEB J., 17, 876–898.

  • Takahashi K, Saishin Y, Saishin Y, Mori K, Ando A, Yamamoto S, Oshima Y, Nambu H, Melia MB, Bingaman DP and Campochiaro PA . (2003b). Invest. Ophthalmol. Vis. Sci., 44, 409–415.

  • Takahashi T, Nakamura T, Hayashi A, Kamei M, Nakabayashi M, Okada AA, Tomita N, Daneda Y and Tano Y . (2000). Am. J. Ophthalmol., 130, 774–781.

  • Takano S, Toshii Y, Kondo S, Suzuki H, Maruno T, Shirai S and Nose T . (1996). Cancer Res, 56, 2185–2190.

  • Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, Glazer N, Holash J, McDonald DM and Yancopoulos GD . (2000). Nat. Med., 6, 460–463.

  • Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD and McDonald DM . (1999). Science, 286, 2511–2515.

  • Tobe T, Ortega S, Luna L, Ozaki H, Okamoto N, Derevjanik NL, Vinores SA, Basilico C and Campochiaro PA . (1998). Am. J. Pathol., 153, 1641–1646.

  • Tolentino MJ, Miller JW, Gragoudas ES, Jakobiec FA, Flynn E, Chatzistefanou K, Ferrara N and Adamis AP . (1996). Ophthalmology, 103, 1820–1828.

  • Tombran-Tink J, Chader GG and Johnson SV . (1991). Exp. Eye Res., 53, 411–414.

  • Tozer GM, Prise VE, Wilson J, Locke RJ, Vojnovic B, Stratford MRL, Dennis MF and Chaplin DJ . (1999). Cancer Res, 59, 1626–1634.

  • Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M and DuBois RN . (1998). Cell, 93, 705–716.

  • Visconti RP, Richardson CD and Sato TN . (2002). Proc. Natil. Acad. Sci. USA, 99, 8219–8224.

  • Watanabe T and Raff MC . (1988). Nature, 332, 834–837.

  • Williams CS, Mann M and DuBois RN . (1999). Oncogene, 18, 7908–7916.

  • Williams CS, Tsujii M, Reese J, Dey SK and DuBois RN . (2000). J. Clin. Invest., 105, 1589–1594.

  • Witzenbichler B, Maisonpierre PC, Jones P, Yancopoulos GD and Isner JM . (1998). J. Biol. Chem., 213, 18514–18521.

  • Woods JA, Hatfield JA, Pettit GR, Fox BW and McGown AT . (1995). Br. J. Cancer, 71, 705–711.

  • Wright AD, Kohner EM, Oakley NW, Hartog M, Joplin GF and Fraser TR . (1969). Br. Med. J., 2, 346–348.

  • Yamada E, Tobe T, Yamada H, Okamoto N, Zack DJ, Werb Z, Soloway P and Campochiaro PA . (2001). Histol. Histopathol., 16, 87–97.

  • Yamada H, Yamada E, Kwak N, Ando A, Suzuki A, Esumi N, Zack DJ and Campochiaro PA . (2000). J. Cell. Physiol., 185, 135–142.

  • Yamada M, Kawai M, Kawai Y and Mashima Y . (1999). Curr. Eye Res., 19, 300–304.

  • Ziche M, Jones J and Gullino PM . (1982). J. Natl. Cancer Inst., 69, 475–482.

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Acknowledgements

Supported by EY05951, EY12609, and core grant P30EY1765 from the NEI; Research to Prevent Blindness, Inc (a Lew R Wasserman Merit Award (PAC)); Dr and Mrs William Lake. PAC is the George S and Dolores Dore Eccles Professor of Ophthalmology.

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  1. The Departments of Ophthalmology and Neuroscience, The Johns Hopkins University School of Medicine, Maumenee 719, 600 N. Wolfe Street, Baltimore, 21287-9277, MD, USA

    Peter Anthony Campochiaro & Sean Francis Hackett

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Campochiaro, P., Hackett, S. Ocular neovascularization: a valuable model system. Oncogene 22, 6537–6548 (2003). https://doi.org/10.1038/sj.onc.1206773

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