Proteolytic processing regulates placental growth factor activities

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 17976-17989

  Hoffmann, Daniel C ^a   Willenborg, Sebastian ^a   Koch, Manuel ^a,b   Zwolanek, Daniela ^b   Müller, Stefan ^b   Becker, Ann Kathrin A ^a   Metzger, Stephanie ^c   Ehrbar, Martin ^c   Kurschat, Peter ^a   Hellmich, Martin ^a   Hubbell, Jeffrey A ^d   Eming, Sabine A ^a,b,e  

^a UNIVERSITY OF COLOGNE   (Germany)

^b Center for Biochemistry   (Germany)

^c Institute of Medical Statistics   (Germany)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYL-TERMINAL; GROWTH FACTOR; HEPARIN BINDING; PROTEOLYTIC PROCESSING; VASCULARIZATION; VESSEL FORMATION;

BLOOD VESSELS;

BIOACTIVITY;

HEPARIN; NEUROPILIN 1; PLACENTAL GROWTH FACTOR; PLACENTAL GROWTH FACTOR 1; PLACENTAL GROWTH FACTOR 118; PLACENTAL GROWTH FACTOR 2; PLASMIN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; GRANULATION TISSUE; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROCESSING; REGULATORY MECHANISM; SKIN INJURY;

ANGIOGENESIS; MECHANISM OF GROWTH FACTOR REGULATION; PLASMIN; PLGF; PROTEASE; VASCULAR BIOLOGY; VASCULAR ENDOTHELIAL GROWTH FACTOR (VEGF);

ANIMALS; BINDING SITES; BLOTTING, WESTERN; ENDOTHELIAL CELLS; FEMALE; FIBRINOLYSIN; HEK293 CELLS; HEPARIN; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROPILIN-1; PHOSPHORYLATION; PLACENTA; PREGNANCY; PREGNANCY PROTEINS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEOLYSIS; SF9 CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84880079373     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.451831     Document Type: Article

References (43)

1. Cianfarani, F., Zambruno, G., Brogelli, L., Sera, F., Lacal, P. M., Pesce, M., Capogrossi, M. C., Failla, C. M., Napolitano, M., and Odorisio, T. (2006) Placenta growth factor in diabetic wound healing. Altered expression and therapeutic potential. Am. J. Pathol. 169, 1167-1182 (Pubitemid 351194354)
2. Gargioli, C., Coletta, M., De Grandis, F., Cannata, S. M., and Cossu, G. (2008) PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat. Med. 14, 973-978
3. Iwasaki, H., Kawamoto, A., Tjwa, M., Horii, M., Hayashi, S., Oyamada, A., Matsumoto, T., Suehiro, S., Carmeliet, P., and Asahara, T. (2011) PlGF repairs myocardial ischemia through mechanisms of angiogenesis, cardioprotection and recruitment of myo-angiogenic competent marrow progenitors. PLoS One 6, e24872
4. Maes, C., Coenegrachts, L., Stockmans, I., Daci, E., Luttun, A., Petryk, A., Gopalakrishnan, R., Moermans, K., Smets, N., Verfaillie, C. M., Carmeliet, P., Bouillon, R., and Carmeliet, G. (2006) Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J. Clin. Invest. 116, 1230-1242
5. Oura, H., Bertoncini, J., Velasco, P., Brown, L. F., Carmeliet, P., and Detmar, M. (2003)Acritical role of placental growth factor in the induction of inflammation and edema formation. Blood 101, 560-567 (Pubitemid 36077578)
6. Van de Veire, S., Stalmans, I., Heindryckx, F., Oura, H., Tijeras-Raballand, A., Schmidt, T., Loges, S., Albrecht, I., Jonckx, B., Vinckier, S., Van Steenkiste, C., Tugues, S., Rolny, C., De Mol, M., Dettori, D., Hainaud, P., Coenegrachts, L., Contreres, J. O., Van Bergen, T., Cuervo, H., Xiao, W. H., Le Henaff, C., Buysschaert, I., Kharabi Masouleh, B., Geerts, A., Schomber, T., Bonnin, P., Lambert, V., Haustraete, J., Zacchigna, S., Rakic, J. M., Jiménez, W., Noël, A., Giacca, M., Colle, I., Foidart, J. M., Tobelem, G., Morales-Ruiz, M., Vilar, J., Maxwell, P., Vinores, S. A., Carmeliet, G., Dewerchin, M., Claesson-Welsh, L., Dupuy, E., Van Vlierberghe, H., Christofori, G., Mazzone, M., Detmar, M., Collen, D., and Carmeliet, P. (2010) Further pharmacological and genetic evidence for the efficacy of PlGF inhibition in cancer and eye disease. Cell 141, 178-190
7. Fischer, C., Mazzone, M., Jonckx, B., and Carmeliet, P. (2008) FLT1 and its ligands VEGFB and PlGF. Drug targets for anti-angiogenic therapy? Nat. Rev. Cancer 8, 942-956
8. Autiero, M., Waltenberger, J., Communi, D., Kranz, A., Moons, L., Lambrechts, D., Kroll, J., Plaisance, S., De Mol, M., Bono, F., Kliche, S., Fellbrich, G., Ballmer-Hofer, K., Maglione, D., Mayr-Beyrle, U., Dewerchin, M., Dombrowski, S., Stanimirovic, D., Van Hummelen, P., Dehio, C., Hicklin, D. J., Persico, G., Herbert, J. M., Communi, D., Shibuya, M., Collen, D., Conway, E. M., and Carmeliet, P. (2003) Role of PlGF in the intraand intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat. Med. 9, 936-943 (Pubitemid 36889938)
9. 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., Di-Palma, T., Dewerchin, M., Noel, A., Stalmans, I., Barra, A., Blacher, S., VandenDriessche, T., Ponten, A., Eriksson, U., Plate, K. H., Foidart, J. M., Schaper, W., Charnock-Jones, D. S., Hicklin, D. J., Herbert, J. M., Collen, D., and Persico, M. G. (2001) Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat. Med. 7, 575-583 (Pubitemid 32448325)
10. Hattori, K., Heissig, B., Wu, Y., Dias, S., Tejada, R., Ferris, B., Hicklin, D. J., Zhu, Z., Bohlen, P., Witte, L., Hendrikx, J., Hackett, N. R., Crystal, R. G., Moore, M. A., Werb, Z., Lyden, D., and Rafii, S. (2002) Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1 + stem cells from bone-marrow microenvironment. Nat. Med. 8, 841-849
11. Ferrara, N. (2004) Vascular endothelial growth factor. Basic science and clinical progress. Endocr. Rev. 25, 581-611 (Pubitemid 39099316)
12. Maglione, D., Guerriero, V., Viglietto, G., Ferraro, M. G., Aprelikova, O., Alitalo, K., Del Vecchio, S., Lei, K. J., Chou, J. Y., and Persico, M. G. (1993) Two alternative mRNAs coding for the angiogenic factor, placenta growth factor (PlGF), are transcribed from a single gene of chromosome 14. Oncogene 8, 925-931 (Pubitemid 23087424)
13. DiPalma, T., Tucci, M., Russo, G., Maglione, D., Lago, C. T., Romano, A., Saccone, S., Della Valle, G., De Gregorio, L., Dragani, T. A., Viglietto, G., and Persico, M. G. (1996) The placenta growth factor gene of the mouse. Mamm. Genome 7, 6-12 (Pubitemid 126439700)
14. Hauser, S., and Weich, H. A. (1993) A heparin-binding form of placenta growth factor (PlGF-2) is expressed in human umbilical vein endothelial cells and in placenta. Growth Factors 9, 259-268 (Pubitemid 24034347)
15. Mamluk, R., Gechtman, Z., Kutcher, M. E., Gasiunas, N., Gallagher, J., and Klagsbrun, M. (2002) Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J. Biol. Chem. 277, 24818-34825
16. Migdal, M., Huppertz, B., Tessler, S., Comforti, A., Shibuya, M., Reich, R., Baumann, H., and Neufeld, G. (1998) Neuropilin-1 is a placenta growth factor-2 receptor. J. Biol. Chem. 273, 22272-22278 (Pubitemid 28399784)
17. Kawamura, H., Li, X., Goishi, K., van Meeteren, L. A., Jakobsson, L., Cébe-Suarez, S., Shimizu, A., Edholm, D., Ballmer-Hofer, K., Kjellén, L., Klagsbrun, M., and Claesson-Welsh, L. (2008) Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood 112, 3638-3649
18. Soker, S., Fidder, H., Neufeld, G., and Klagsbrun, M. (1996) Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J. Biol. Chem. 271, 5761-5767
19. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D., and Betsholtz, C. (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (Pubitemid 36870177)
20. Ruhrberg, C., Gerhardt, H., Golding, M., Watson, R., Ioannidou, S., Fujisawa, H., Betsholtz, C., and Shima, D. T. (2002) Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16, 2684-2698
21. Houck, K. A., Leung, D. W., Rowland, A. M., Winer, J., and Ferrara, N. (1992) Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 267, 26031-26037 (Pubitemid 23014012)
22. Keyt, B. A., Berleau, L. T., Nguyen, H. V., Chen, H., Heinsohn, H., Vandlen, R., and Ferrara, N. (1996) The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem. 271, 7788-779523.
23. Lauer, G., Sollberg, S., Cole, M., Flamme, I., Stürzebecher, J., Mann, K., Krieg, T., and Eming, S. A. (2000) Expression and proteolysis of vascular endothelial growth factor is increased in chronic wounds. J. Invest. Dermatol. 115, 12-18 (Pubitemid 30470185)
24. Lee, S., Jilani, S. M., Nikolova, G. V., Carpizo, D., and Iruela-Arispe, M. L. (2005) Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J. Cell Biol. 169, 681-691 (Pubitemid 41002860)
25. Roth, D., Piekarek, M., Paulsson, M., Christ, H., Bloch, W., Krieg, T., Davidson, J. M., and Eming, S. A. (2006) Plasmin modulates vascular endothelial growth factor-A-mediated angiogenesis during wound repair. Am. J. Pathol. 168, 670-684 (Pubitemid 43271164)
26. Ricard-Blum, S., Féraud, O., Lortat-Jacob, H., Rencurosi, A., Fukai, N., Dkhissi, F., Vittet, D., Imberty, A., Olsen, B. R., and van der Rest, M. (2004) Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling. J. Biol. Chem. 279, 2927-2936 (Pubitemid 38114285)
27. Eming, S. A., Smola-Hess, S., Kurschat, P., Hirche, D., Krieg, T., and Smola, H. (2006) A novel property of povidon-iodine. Inhibition of excessive protease levels in chronic non-healing wounds. J. Invest. Dermatol. 126, 2731-2733 (Pubitemid 44764062)
28. Palolahti, M., Lauharanta, J., Stephens, R. W., Kuusela, P., and Vaheri, A. (1993) Proteolytic activity in leg ulcer exudate. Exp. Dermatol. 2, 29-37 (Pubitemid 23244485)
29. Joukov, V., Sorsa, T., Kumar, V., Jeltsch, M., Claesson-Welsh, L., Cao, Y., Saksela, O., Kalkkinen, N., and Alitalo, K. (1997) Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 16, 3898-3911 (Pubitemid 27281006)
30. Sawano, A., Takahashi, T., Yamaguchi, S., Aonuma, M., and Shibuya, M. (1996) Flt-1 but not KDR/Flk-1 tyrosine kinase is a receptor for placenta growth factor, which is related to vascular endothelial growth factor. Cell Growth Differ. 7, 213-221 (Pubitemid 26049830)
31. Herzog, B., Pellet-Many, C., Britton, G., Hartzoulakis, B., and Zachary, I. C. (2011) VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation. Mol. Biol. Cell 22, 2766-2776
32. Zachary, I. C. (2011) How neuropilin-1 regulates receptor tyrosine kinase signalling. The knowns and known unknowns. Biochem. Soc. Trans. 39, 1583-1591
33. Grünewald, F. S., Prota, A. E., Giese, A., and Ballmer-Hofer, K. (2010) Structure-function analysis of VEGF receptor activation and the role of coreceptors in angiogenic signaling. Biochim. Biophys. Acta. 1804, 567-580
34. Cébe-Suarez, S., Grünewald, F. S., Jaussi, R., Li, X., Claesson-Welsh, L., Spillmann, D., Mercer, A. A., Prota, A. E., and Ballmer-Hofer, K. (2008) Orf virus VEGF-E NZ2 promotes paracellular NRP-1/VEGFR-2 coreceptor assembly via the peptide RPPR. FASEB J. 22, 3078-3086
35. Vander Kooi, C. W., Jusino, M. A., Perman, B., Neau, D. B., Bellamy, H. D., and Leahy, D. J. (2007) Structural basis for ligand and heparin binding to neuropilin B domains. Proc. Natl. Acad. Sci. U.S.A. 104, 6152-6157 (Pubitemid 47186064)
36. Parker, M. W., Xu, P., Li, X., and Vander Kooi, C. W. (2012) Structural basis for selective vascular endothelial growth factor-A (VEGF-A) binding to neuropilin-1. J. Biol. Chem. 287, 11082-11089
37. Ballmer-Hofer, K., Andersson, A. E., Ratcliffe, L. E., and Berger, P. (2011) Neuropilin-1 promotes VEGFR-2 trafficking through Rab11 vesicles thereby specifying signal output. Blood 118, 816-826
38. Pan, Q., Chathery, Y., Wu, Y., Rathore, N., Tong, R. K., Peale, F., Bagri, A., Tessier-Lavigne, M., Koch, A. W., and Watts, R. J. (2007) Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J. Biol. Chem. 282, 24049-24056 (Pubitemid 47328044)
39. von Wronski, M. A., Raju, N., Pillai, R., Bogdan, N. J., Marinelli, E. R., Nanjappan, P., Ramalingam, K., Arunachalam, T., Eaton, S., Linder, K. E., Yan, F., Pochon, S., Tweedle, M. F., and Nunn, A. D. (2006) Tuftsin binds neuropilin-1 through a sequence similar to that encoded by exon 8 of vascular endothelial growth factor. J. Biol. Chem. 281, 5702-5710 (Pubitemid 43847668)
40. Abu-Ghazaleh, R., Kabir, J., Jia, H., Lobo, M., and Zachary, I. (2001) Src mediates stimulation by vascular endothelial growth factor of the phosphorylation of focal adhesion kinase at tyrosine 861, and migration and anti-apoptosis in endothelial cells. Biochem. J. 360, 255-264 (Pubitemid 33081972)
41. Shintani, Y., Takashima, S., Asano, Y., Kato, H., Liao, Y., Yamazaki, S., Tsukamoto, O., Seguchi, O., Yamamoto, H., Fukushima, T., Sugahara, K., Kitakaze, M., and Hori, M. (2006) Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling. EMBO J. 25, 3045-3055 (Pubitemid 44106757)
42. Ylä-Herttuala, S., and Alitalo, K. (2003) Gene transfer as a tool to induce therapeutic vascular growth. Nat. Med. 9, 694-701 (Pubitemid 36749218)
43. Luttun, A., Tjwa, M., Moons, L., Wu, Y., Angelillo-Scherrer, A., Liao, F., Nagy, J. A., Hooper, A., Priller, J., De Klerck, B., Compernolle, V., Daci, E., Bohlen, P., Dewerchin, M., Herbert, J. M., Fava, R., Matthys, P., Carmeliet, G., Collen, D., Dvorak, H. F., Hicklin, D. J., and Carmeliet, P. (2002) Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat. Med. 8, 831-840