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Angiogenesis and parasitic helminth-associated neovascularization

Published online by Cambridge University Press:  14 January 2011

ROGER D. DENNIS ,
UWE SCHUBERT  and
CHRISTIAN BAUER
ROGER D. DENNIS*
Affiliation:
Institute for Biochemistry, Justus Liebig University Giessen, Friedrichstrasse 24, 35392 Giessen, Germany
UWE SCHUBERT
Affiliation:
Institute for Biochemistry, Justus Liebig University Giessen, Friedrichstrasse 24, 35392 Giessen, Germany
CHRISTIAN BAUER
Affiliation:
Institute of Parasitology, Justus Liebig University Giessen, Rudolf-Buchheim-Strasse 2, 35392 Giessen, Germany
*
*Corresponding author: Institute for Biochemistry, Justus Liebig University Giessen, Friedrichstrasse 24, 35392 Giessen, Germany. Tel: +49 641 99 47460. Fax: +49 641 99 47509. E-mail: roger.d.dennis@googlemail.com and roger.d.dennis@biochemie.med.uni-giessen.de
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Summary

Successful metazoan parasitism, among many other factors, requires a supply of nutrients and the removal of waste products. There is a prerequisite for a parasite-defined vasculature. The angiogenic mechanism(s) involved presumably depend on the characteristics of the tissue- and vascular system-dwelling, parasitic helminths. Simplistically, 2 possibilities or a combination of both have been considered in this review. The multifactorial induction of parasitic helminth-associated neovascularization could arise through, either a host-, a parasite- or a host-/parasite-dependent, angiogenic switch. Most studies appear to support the first and third hypotheses, but evidence exists for the intrahepatic cestode Echinococcus multilocularis, the free-living nematode Caenorhabditis elegans and the intravascular trematode Schistosoma mansoni for the second inference. In contrast, the nematode anti-coagulant protein NAPc2 from adult Ancylostoma caninum is also an anti-angiogenic factor.

Keywords

angiogenesisangiogenic switchangiogenic growth factorVEGFparasitic helminth-associated neovascularizationCestodaNematodaTrematoda
Type
Review Article
Information
Parasitology , Volume 138 , Issue 4 , April 2011 , pp. 426 - 439
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Ackley, B. D., Crew, J. R., Elamaa, H., Pihlajaniemi, T., Kuo, C. J. and Kramer, J. M. (2001). The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. The Journal of Cell Biology 152, 1219–1232.Google Scholar
Adams, R. H. and Alitalo, K. (2007). Molecular regulation of angiogenesis and lymphangiogenesis. Nature Reviews Molecular Cell Biology 8, 464–478.Google Scholar
Aguilar-Diaz, H., Bobes, R. J., Carrero, J. C., Camacho-Carranza, R., Cervantes, C., Cevallos, M. A., Davila, G., Rodriguez-Dorantes, M., Escobedo, G., Fernandez, J. L., Fragoso, G., Gaytan, P., Garciarubio, A., Gonzalez, V. M., Gonzalez, L., Jose, M. V., Jimenez, L., Laclette, J. P., Landa, A., Larralde, C., Morales-Montor, J., Morett, E., Ostoa-Saloma, P., Sciutto, E., Santamaria, R. I., Soberon, X., de la Torre, P., Valdes, V. and Yanez, J. (2006). The genome project of Taenia solium. Parasitology International 55 (Suppl.) S127–S130.CrossRefGoogle ScholarPubMed
Akagami, M., Nakamura, K., Nishino, H., Seki, S., Shimizu, H. and Yamamoto, Y. (2010). Pathogenesis of venous hypertrophy associated with schistosomiasis in whooper swans (Cygnus cygnus) in Japan. Avian Diseases 54, 146–150.CrossRefGoogle ScholarPubMed
Alitalo, K., Tammela, T. and Petrova, T. V. (2005). Lymphangiogenesis in development and human disease. Nature, London 438 (7070), 946–953.Google Scholar
Alvarez, J. I., Colegial, C. H., Castano, C. A., Trujillo, J., Teale, J. M. and Restrepo, B. I. (2002). The human nervous tissue in proximity to granulomatous lesions induced by Taenia solium metacestodes displays an active response. Journal of Neuroimmunology 127, 139–144.CrossRefGoogle ScholarPubMed
Alvarez, J. I. and Teale, J. M. (2006). Breakdown of the blood brain barrier and blood-cerebrospinal fluid barrier is associated with differential leukocyte migration in distinct compartments of the CNS during the course of murine NCC. Journal of Neuroimmunology 173, 45–55.CrossRefGoogle ScholarPubMed
Andrade, Z. A. (2009). Schistosomiasis and liver fibrosis. Parasite Immunology 31, 656–663.CrossRefGoogle ScholarPubMed
Andrade, Z. A. and Cheever, A. W. (1971). Alterations of the intrahepatic vasculature in hepatosplenic schistosomiasis mansoni. American Journal of Tropical Medicine and Hygiene 20, 425–432.CrossRefGoogle ScholarPubMed
Attout, T., Hoerauf, A., Denece, G., Debrah, A. Y., Marfo-Debrekyei, Y., Boussinesq, M., Wanji, S., Martinez, V., Mand, S., Adjei, O., Bain, O., Specht, S. and Martin, C. (2009). Lymphatic vascularisation and involvement of Lyve-1+ macrophages in the human onchocerca nodule. PLoS One 4, e8234.CrossRefGoogle ScholarPubMed
Bahnemann, R. and Bauer, C. (1994). Lungworm infection in a beagle colony: Filaroides hirthi, a common but not well-known companion. Experimental and Toxicologic Pathology 46, 55–62.CrossRefGoogle Scholar
Baptista, A. P. and Andrade, Z. A. (2005). Angiogenesis and schistosomal granuloma formation. Memórias do Instituto Oswaldo Cruz 100, 183–185.CrossRefGoogle ScholarPubMed
Baruch, A. M. and Despommier, D. D. (1991). Blood vessels in Trichinella spiralis infections: a study using vascular casts. Journal of Parasitology 77, 99–103.Google Scholar
Bennuru, S. and Nutman, T. B. (2009). Lymphangiogenesis and lymphatic remodeling induced by filarial parasites: implications for pathogenesis. PLoS Pathogens 5, e1000688.CrossRefGoogle ScholarPubMed
Bergers, G. and Benjamin, L. E. (2003). Tumorigenesis and the angiogenic switch. Nature Reviews Cancer 3, 401–410.Google Scholar
Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z. and Hanahan, D. (2000). Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nature Cell Biology 2, 737–744.Google Scholar
Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature, London 460 (7253), 352–358.CrossRefGoogle ScholarPubMed
Birnbaum, D., Popovici, C. and Roubin, R. (2005). A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Developmental Dynamics 232, 247–255.CrossRefGoogle ScholarPubMed
Bloch, E. H., Wahab, M. F. and Warren, K. S. (1972). In vivo microscopic observations of the pathogenesis and pathophysiology of hepatosplenic schistosomiasis in the mouse liver. American Journal of Tropical Medicine and Hygiene 21, 546–557.CrossRefGoogle ScholarPubMed
Bogliolo, L. (1957). The anatomical picture of the liver in hepato-splenic schistosomiasis mansoni. Annals of Tropical Medicine and Parasitology 51, 1–14.CrossRefGoogle ScholarPubMed
Bolt, G., Monrad, J., Koch, J. and Jensen, A. L. (1994). Canine angiostrongylosis: a review. Veterinary Record 135, 447–452.CrossRefGoogle ScholarPubMed
Botros, S. S., Hammam, O. A., El-Lakkany, N. M., El-Din, S. H. and Ebeid, F. A. (2008). Schistosoma haematobium (Egyptian strain): rate of development and effect of praziquantel treatment. Journal of Parasitology 94, 386–394.CrossRefGoogle ScholarPubMed
Bourque, A. C., Conboy, G., Miller, L. M. and Whitney, H. (2008). Pathological findings in dogs naturally infected with Angiostrongylus vasorum in Newfoundland and Labrador, Canada. Journal of Veterinary Diagnostic Investigation 20, 11–20.CrossRefGoogle ScholarPubMed
C.elegans, S. C. (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282 (5396), 2012–2018.Google Scholar
Capo, V. A., Despommier, D. D. and Polvere, R. I. (1998). Trichinella spiralis: vascular endothelial growth factor is up-regulated within the nurse cell during the early phase of its formation. Journal of Parasitology 84, 209–214.CrossRefGoogle ScholarPubMed
Cappello, M., Vlasuk, G. P., Bergum, P. W., Huang, S. and Hotez, P. J. (1995). Ancylostoma caninum anticoagulant peptide: a hookworm-derived inhibitor of human coagulation factor Xa. Proceedings of the National Academy of Sciences, USA 92, 6152–6156.CrossRefGoogle ScholarPubMed
Carmeliet, P. (2000). Mechanisms of angiogenesis and arteriogenesis. Nature Medicine 6, 389–395.Google Scholar
Carmeliet, P. (2003). Angiogenesis in health and disease. Nature Medicine 9, 653–660.CrossRefGoogle ScholarPubMed
Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature, London 438 (7070), 932–936.Google Scholar
Collins, R. C., Lujan, R., Figueroa, H. and Campbell, C. C. (1982). Early formation of the nodule in Guatemalan onchocerciasis. American Journal of Tropical Medicine and Hygiene 31, 267–269.Google Scholar
Coulier, F., Pontarotti, P., Roubin, R., Hartung, H., Goldfarb, M. and Birnbaum, D. (1997). Of worms and men: an evolutionary perspective on the fibroblast growth factor (FGF) and FGF receptor families. Journal of Molecular Evolution 44, 43–56.CrossRefGoogle ScholarPubMed
Coultas, L., Chawengsaksophak, K. and Rossant, J. (2005). Endothelial cells and VEGF in vascular development. Nature, London 438 (7070), 937–945.CrossRefGoogle ScholarPubMed
Debrah, A. Y., Mand, S., Marfo-Debrekyei, Y., Batsa, L., Pfarr, K., Lawson, B., Taylor, M., Adjei, O. and Hoerauf, A. (2009). Reduction in levels of plasma vascular endothelial growth factor-A and improvement in hydrocele patients by targeting endosymbiotic Wolbachia sp. in Wuchereria bancrofti with doxycycline. American Journal of Tropical Medicine and Hygiene 80, 956–963.Google Scholar
Debrah, A. Y., Mand, S., Specht, S., Marfo-Debrekyei, Y., Batsa, L., Pfarr, K., Larbi, J., Lawson, B., Taylor, M., Adjei, O. and Hoerauf, A. (2006). Doxycycline reduces plasma VEGF-C/sVEGFR-3 and improves pathology in lymphatic filariasis. PLoS Pathogens 2, e92.Google Scholar
Debrah, A. Y., Mand, S., Toliat, M. R., Marfo-Debrekyei, Y., Batsa, L., Nurnberg, P., Lawson, B., Adjei, O., Hoerauf, A. and Pfarr, K. (2007). Plasma vascular endothelial growth Factor-A (VEGF-A) and VEGF-A gene polymorphism are associated with hydrocele development in lymphatic filariasis. American Journal of Tropical Medicine and Hygiene 77, 601–608.Google Scholar
Dennis, R. D., Geyer, H. and Geyer, R. (2007). Glycoconjugates of parasitic helminth infections. In Comprehensive Glycosciences, Vol. 4 (ed. Kamerling, J. P.), pp. 473–494. Elsevier, Amsterdam, The Netherlands.CrossRefGoogle Scholar
De Souza, M. M., Tolentino, M. Jr., Assis, B. C., Cristina De Oliveira Gonzalez, A., Maria Correia Silva, T. and Andrade, Z. A. (2006). Pathogenesis of septal fibrosis of the liver. (An experimental study with a new model). Pathology, Research and Practice 202, 883–889.CrossRefGoogle Scholar
Despommier, D. D. (1990). Trichinella spiralis: the worm that would be virus. Parasitology Today 6 193–196.CrossRefGoogle ScholarPubMed
Despommier, D. D. (1993). Trichinella spiralis and the concept of niche. Journal of Parasitology 79 472–482.CrossRefGoogle ScholarPubMed
Despommier, D. D. (1998). How does Trichinella spiralis make itself at home? Parasitology Today 14, 318–323.CrossRefGoogle ScholarPubMed
Dreyer, G., Noroes, J., Figueredo-Silva, J. and Piessens, W. F. (2000). Pathogenesis of lymphatic disease in bancroftian filariasis: a clinical perspective. Parasitology Today 16, 544–548.Google Scholar
Dunn, M. A., Mansour, M. M., Guindy, S. and Rojkind, M. (1986). Liver fibroblast proliferation in murine schistosomiasis. American Journal of Tropical Medicine and Hygiene 35, 1185–1191.Google Scholar
Edison, A. S. (2009). Caenorhabditis elegans pheromones regulate multiple complex behaviors. Current Opinion in Neurobiology 19, 378–388.CrossRefGoogle ScholarPubMed
El-Awady, M. K., Gad, Y. Z., Wen, Y., Eassawi, M., Effat, L., Amr, K. S., Ismail, S. and Christ, G. J. (2001). Schistosoma hematobium soluble egg antigens induce proliferation of urothelial and endothelial cells. World Journal Urology 19, 263–266.Google Scholar
El-Sobky, E., Gomha, M., El-Baz, M., Abol-Enein, H. and Shaaban, A. A. (2002). Prognostic significance of tumour angiogenesis in schistosoma-associated adenocarcinoma of the urinary bladder. BJU International 89, 126–132.Google ScholarPubMed
Elsobky, E., El-Baz, M., Gomha, M., Abol-Enein, H. and Shaaban, A. A. (2002). Prognostic value of angiogenesis in schistosoma-associated squamous cell carcinoma of the urinary bladder. Urology 60, 69–73.Google Scholar
Esterre, P., Plichart, C., Huin-Blondey, M. O. and Nguyen, L. N. (2005). Soluble cellular adhesion molecules, selectins, VEGF and endothelin-1 in patients with Wuchereria bancrofti infection and association with clinical status. Parasite Immunology 27, 9–16.Google Scholar
Fainaru, O., Hornstein, M. D. and Folkman, J. (2009). Doxycycline inhibits vascular leakage and prevents ovarian hyperstimulation syndrome in a murine model. Fertility and Sterility 92, 1701–1705.CrossRefGoogle ScholarPubMed
Ferrara, N. (2009). Vascular endothelial growth factor. Arteriosclerosis,Thrombosis, and Vascular Biology 29, 789–791.Google Scholar
Ferrara, N., Gerber, H. P. and LeCouter, J. (2003). The biology of VEGF and its receptors. Nature Medicine 9, 669–676.CrossRefGoogle ScholarPubMed
Ferrara, N. and Kerbel, R. S. (2005). Angiogenesis as a therapeutic target. Nature, London 438 (7070), 967–974.Google Scholar
File, S. (1995). Interaction of schistosome eggs with vascular endothelium. Journal of Parasitology 81, 234–238.Google Scholar
Freedman, D. O. and Ottesen, E. A. (1988). Eggs of Schistosoma mansoni stimulate endothelial cell proliferation in vitro. Journal of Infectious Diseases 158, 556–562.Google Scholar
Galuska, S. P., Rollenhagen, M., Kaup, M., Eggers, K., Oltmann-Norden, I., Schiff, M., Hartmann, M., Weinhold, B., Hildebrandt, H., Geyer, R., Muhlenhoff, M. and Geyer, H. (2010). Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proceedings of the National Academy of Sciences, USA 107, 10250–10255.Google Scholar
George, G. H., Palmieri, J. R. and Connor, D. H. (1985). The onchocercal nodule: interrelationship of adult worms and blood vessels. American Journal of Tropical Medicine and Hygiene 34, 1144–1148.Google Scholar
Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V., Creasy, T., Amedeo, P., Haas, B., El-Sayed, N. M., Wortman, J. R., Feldblyum, T., Tallon, L., Schatz, M., Shumway, M., Koo, H., Salzberg, S. L., Schobel, S., Pertea, M., Pop, M., White, O., Barton, G. J., Carlow, C. K., Crawford, M. J., Daub, J., Dimmic, M. W., Estes, C. F., Foster, J. M., Ganatra, M., Gregory, W. F., Johnson, N. M., Jin, J., Komuniecki, R., Korf, I., Kumar, S., Laney, S., Li, B. W., Li, W., Lindblom, T. H., Lustigman, S., Ma, D., Maina, C. V., Martin, D. M., McCarter, J. P., McReynolds, L., Mitreva, M., Nutman, T. B., Parkinson, J., Peregrin-Alvarez, J. M., Poole, C., Ren, Q., Saunders, L., Sluder, A. E., Smith, K., Stanke, M., Unnasch, T. R., Ware, J., Wei, A. D., Weil, G., Williams, D. J., Zhang, Y., Williams, S. A., Fraser-Liggett, C., Slatko, B., Blaxter, M. L. and Scott, A. L. (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 317 (5845), 1756–1760.CrossRefGoogle ScholarPubMed
Grandi, G., Zivicnjak, T. and Beck, R. (2007). Pathogenesis of Dirofilaria spp. infections. In Dirofilaria immitis and D. repens in Dog and Cat and Human Infections (ed. Genchi, C., Rinaldi, L. and Cringoli, G.), Mappe Parassitologiche 8, 59–66.Google Scholar
Guerret, S., Vuitton, D. A., Liance, M., Pater, C. and Carbillet, J. P. (1998). Echinococcus multilocularis: relationship between susceptibility/resistance and liver fibrogenesis in experimental mice. Parasitology Research 84, 657–667.Google Scholar
Hall, L. R., Berger, R. B., Diaconu, E. and Pearlman, E. (2002). Onchocerca volvulus keratitis (river blindness) is exacerbated in BALB/c IL-4 gene knockout mice. Cellular Immunology 216, 1–5.Google Scholar
Hembrough, T. A., Swartz, G. M., Papathanassiu, A., Vlasuk, G. P., Rote, W. E., Green, S. J. and Pribluda, V. S. (2003). Tissue factor/factor VIIa inhibitors block angiogenesis and tumor growth through a nonhemostatic mechanism. Cancer Research 63, 2997–3000.Google Scholar
Higazi, T. B., Pearlman, E., Whikehart, D. R. and Unnasch, T. R. (2003). Angiogenic activity of an Onchocerca volvulus Ancylostoma secreted protein homologue. Molecular and Biochemical Parasitology 129, 61–68.Google Scholar
Hiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., Shipley, J. M., Senior, R. M. and Shibuya, M. (2002). MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2, 289–300.Google Scholar
Hirth, R. S. and Hottendorf, G. H. (1973). Lesions produced by a new lungworm in beagle dogs. Veterinary Pathology 10, 385–407.Google Scholar
Ho, Q. T. and Kuo, C. J. (2007). Vascular endothelial growth factor: biology and therapeutic applications. The International Journal of Biochemistry and Cell Biology 39, 1349–1357.CrossRefGoogle ScholarPubMed
Humes, A. G. and Akers, R. P. (1952). Vascular changes in the cheek pouch of the golden hamster during infection with Trichinella spiralis larvae. The Anatomical Record 114, 103–113.CrossRefGoogle ScholarPubMed
Inoue, M., Hager, J. H., Ferrara, N., Gerber, H. P. and Hanahan, D. (2002). VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic beta cell carcinogenesis. Cancer Cell 1, 193–202.Google Scholar
Jain, R. K. (2003). Molecular regulation of vessel maturation. Nature Medicine 9, 685–693.Google Scholar
Jain, R. K., Munn, L. L. and Fukumura, D. (2002). Dissecting tumour pathophysiology using intravital microscopy. Nature Reviews Cancer 2, 266–276.Google Scholar
Jiang, X. and Couchman, J. R. (2003). Perlecan and tumor angiogenesis. The Journal of Histochemistry and Cytochemistry 51, 1393–1410.CrossRefGoogle ScholarPubMed
Kanse, S. M., Liang, O., Schubert, U., Haas, H., Preissner, K. T., Doenhoff, M. J. and Dennis, R. D. (2005). Characterisation and partial purification of Schistosoma mansoni egg-derived pro-angiogenic factor. Molecular and Biochemical Parasitology 144, 76–85.Google Scholar
Karamysheva, A. F. (2008). Mechanisms of angiogenesis. Biochemistry (Moscow) 73, 751–762.Google Scholar
Ko, R. C., Fan, L., Lee, D. L. and Compton, H. (1994). Changes in host muscles induced by excretory/secretory products of larval Trichinella spiralis and Trichinella pseudospiralis. Parasitology 108, 195–205.CrossRefGoogle ScholarPubMed
Korff, T. and Augustin, H. G. (1998). Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. The Journal of Cell Biology 143, 1341–1352.CrossRefGoogle ScholarPubMed
Korff, T. and Augustin, H. G. (1999). Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. Journal of Cell Science 112, 3249–3258.Google Scholar
Kuwamura, M., Sawamoto, O., Yamate, J., Aoki, M., Ohnishi, Y. and Kotani, T. (2007). Pulmonary vascular proliferation and lungworm (Stenurus ovatus) in a bottlenose dolphin (Tursiops turncatus). Journal of Veterinary Medical Science 69, 531–533.Google Scholar
Laha, T., Pinlaor, P., Mulvenna, J., Sripa, B., Sripa, M., Smout, M. J., Gasser, R. B., Brindley, P. J. and Loukas, A. (2007). Gene discovery for the carcinogenic human liver fluke, Opisthorchis viverrini. BMC Genomics 8, 189.CrossRefGoogle ScholarPubMed
Lammie, P. J., Cuenco, K. T. and Punkosdy, G. A. (2002). The pathogenesis of filarial lymphedema: is it the worm or is it the host? Annals of the New York Academy of Sciences 979, 131–142.Google Scholar
LeCouter, J., Kowalski, J., Foster, J., Hass, P., Zhang, Z., Dillard-Telm, L., Frantz, G., Rangell, L., DeGuzman, L., Keller, G. A., Peale, F., Gurney, A., Hillan, K. J. and Ferrara, N. (2001). Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature, London 412 (6850), 877–884.Google Scholar
Lee, J. D., Tsai, L. Y., Chen, C. H., Wang, J. J., Hsiao, J. K. and Yen, C. M. (2006). Blood-brain barrier dysfunction occurring in mice infected with Angiostrongylus cantonensis. Acta Tropica 97, 204–211.Google Scholar
Lejoly-Boisseau, H., Appriou, M., Seigneur, M., Pruvost, A., Tribouley-Duret, J. and Tribouley, J. (1999). Schistosoma mansoni: in vitro adhesion of parasite eggs to the vascular endothelium. Subsequent inhibition by a monoclonal antibody directed to a carbohydrate epitope. Experimental Parasitology 91, 20–29.CrossRefGoogle Scholar
Lemos, Q. T. and Andrade, Z. A. (2010). Angiogenesis and experimental hepatic fibrosis. Memórias do Instituto Oswaldo Cruz 105, 611–614.Google Scholar
Lenzi, H. L., Sobral, A. C. and Lenzi, J. A. (1988). Participation of endothelial cells in murine schistosomiasis. Brazilian Journal of Medical and Biological Research 21, 999–1003.Google Scholar
Lenzi, J. A., Mota, E. M., Pelajo-Machado, M., Vale, L. S., Vale, B. S., Andrade, Z. A. and Lenzi, H. L. (2002). Intestinal fibrovascular nodules caused by Schistosoma mansoni infection in Calomys callosus Rengger, 1830 (Rodentia: Cricetidae): a model of concomitant fibrosis and angiogenesis. Memórias do Instituto Oswaldo Cruz 97 (Suppl. 1) 117–127.Google Scholar
Loeffler, D. A., Lundy, S. K., Singh, K. P., Gerard, H. C., Hudson, A. P. and Boros, D. L. (2002). Soluble egg antigens from Schistosoma mansoni induce angiogenesis-related processes by up-regulating vascular endothelial growth factor in human endothelial cells. Journal of Infectious Diseases 185, 1650–1656.Google Scholar
Manfredi, M. T., Di Cerbo, A. and Genchi, M. (2007). Biology of filarial worms parasitizing dogs and cats. In Dirofilaria immitis and D. repens in Dog and Cat and Human Infections (ed. Genchi, C., Rinaldi, L. and Cringoli, G.), Mappe Parassitologiche 8, 39–45.Google Scholar
Marino, F., Giannetto, S., Cavallaro, M., Paradiso, M. L., Bottari, T. and De Vico, G. (2003). Unitubulotestis sardae (Trematoda: Didymozoidae) infection in Atlantic bonito Sarda sarda (Perciformes: Scomberomoridae) in the Ionian and Tyrrhenian Seas: histopathological and SEM investigations. Journal of Submicroscopic Cytology and Pathology 35, 215–220.Google ScholarPubMed
Marx, P. T., Mulder, A. B., Van Den Bergh, F. A., Overbeeke, R., Haanen, C. and Vermes, I. (1999). Apoptosis inducers endotoxin and Fas-ligation enhance the expression of vascular endothelial growth factor in human endothelial cells. Endothelium 6, 335–340.Google Scholar
Mayer, D. A. and Fried, B. (2007). The role of helminth infections in carcinogenesis. Advances in Parasitology 65, 239–296.Google Scholar
Monshizadeh, R., Ashrafzadeh, M. T. and Rumelt, S. (2000). Choroidal neovascular membrane: a late complication of inactive Toxocara chorioretinitis. Retina 20, 219–220.Google Scholar
Mor, F., Quintana, F. J. and Cohen, I. R. (2004). Angiogenesis-inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. Journal of Immunology 172, 4618–4623.Google Scholar
Mori, K., Ohta, K. and Murata, T. (2007). Vasoproliferative tumors of the retina secondary to ocular toxocariasis. Canadian Journal of Ophthalmology 42, 758–759.Google Scholar
Morgan, S. J., Storts, R. W., Stromberg, P. C., Sowa, B. A. and Lay, J. C. (1989). Preliminary investigations on the effects of a Strongylus vulgaris larval extract, mononuclear factors and platelet factors on equine smooth muscle cells in vitro. Veterinary Research Communications 13, 479–489.CrossRefGoogle ScholarPubMed
Morgan, S. J. and Van Houten, D. S. (1990). The ultrastructure of Strongylus vulgaris-mediated equine chronic mesenteric arteritis. Veterinary Research Communications 14, 41–46.Google Scholar
Ngaiza, J. R., Doenhoff, M. J. and Jaffe, E. A. (1993). Schistosoma mansoni egg attachment to cultured human umbilical vein endothelial cells: an in vitro model of an early step of parasite egg excretion. Journal of Infectious Diseases 168, 1576–1580.Google Scholar
Noonan, D. M., De Lerma Barbaro, A., Vannini, N., Mortara, L. and Albini, A. (2008). Inflammation, inflammatory cells and angiogenesis: decisions and indecisions. Cancer Metastasis Reviews 27, 31–40.CrossRefGoogle ScholarPubMed
Noroes, J., Addiss, D., Amaral, F., Coutinho, A., Medeiros, Z. and Dreyer, G. (1996). Occurrence of living adult Wuchereria bancrofti in the scrotal area of men with microfilaraemia. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 55–56.Google Scholar
O'Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W. S., Flynn, E., Birkhead, J. R., Olsen, B. R. and Folkman, J. (1997). Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88, 277–285.CrossRefGoogle ScholarPubMed
O'Reilly, M. S., Holmgren, L., Chen, C. and Folkman, J. (1996). Angiostatin induces and sustains dormancy of human primary tumors in mice. Nature Medicine 2, 689–692.Google Scholar
O'Reilly, M. S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R. A., Moses, M., Lane, W. S., Cao, Y., Sage, E. H. and Folkman, J. (1994). Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79, 315–328.CrossRefGoogle ScholarPubMed
Ogbourne, C. P. and Duncan, J. L. (1977). Strongylus vulgaris in the Horse: its Biology and Veterinary Importance. Commonwealth Agricultural Bureaux, Farnham Royal Bucks, UK.Google Scholar
Oswald, I. P., Eltoum, I., Wynn, T. A., Schwartz, B., Caspar, P., Paulin, D., Sher, A. and James, S. L. (1994 a). Endothelial cells are activated by cytokine treatment to kill an intravascular parasite, Schistosoma mansoni, through the production of nitric oxide. Proceedings of the National Academy of Sciences, USA 91, 999–1003.Google Scholar
Oswald, I. P., Wynn, T. A., Sher, A. and James, S. L. (1994 b). NO as an effector molecule of parasite killing: modulation of its synthesis by cytokines. Comparative Biochemistry and Physiology. Part C: Pharmacology, Toxicology and Endocrinology 108, 11–18.Google Scholar
Pearlman, E., Diaconu, E., Hazlett, F. E. Jr., Merriweather, A. and Unnasch, T. R. (1997). Identification of an epitope of a recombinant Onchocerca volvulus protein that induces corneal pathology. Molecular and Biochemical Parasitology 89, 123–135.Google Scholar
Pearlman, E. and Hall, L. R. (2000). Immune mechanisms in Onchocerca volvulus-mediated corneal disease (river blindness). Parasite Immunology 22, 625–631.Google Scholar
Peixoto, C. A. and Figueiredo-Silva, J. (2001). Fine structure of intrascrotal lymphatic vessels infected by Wuchereria bancrofti adult worms. Journal of Submicroscopic Cytology and Pathology 33, 125–131.Google Scholar
Pepper, M. S. (2001). Extracellular proteolysis and angiogenesis. Thrombosis and Haemostasis 86, 346–355.Google Scholar
Pfarr, K. M., Debrah, A. Y., Specht, S. and Hoerauf, A. (2009). Filariasis and lymphoedema. Parasite Immunology 31, 664–672.Google Scholar
Popovici, C., Isnardon, D., Birnbaum, D. and Roubin, R. (2002). Caenorhabditis elegans receptors related to mammalian vascular endothelial growth factor receptors are expressed in neural cells. Neuroscience Letters 329, 116–120.CrossRefGoogle ScholarPubMed
Prakash, S., Paul, W. E. and Robbins, P. W. (2007). Fibrosin, a novel fibrogenic cytokine, modulates expression of myofibroblasts. Experimental and Molecular Pathology 82, 42–48.Google Scholar
Presta, M., Dell'Era, P., Mitola, S., Moroni, E., Ronca, R. and Rusnati, M. (2005). Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine and Growth Factor Reviews 16, 159–178.Google Scholar
Rao, U. R., Sutton, E. T., Zometa, C. S. and Vickery, A. C. (1996 a). Effect of Brugia malayi infections on endothelial cells: a morphological study. Journal of Submicroscopic Cytology and Pathology 28, 227–241.Google Scholar
Rao, U. R., Zometa, C. S., Vickery, A. C., Kwa, B. H., Nayar, J. K. and Sutton, E. T. (1996 b). Effect of Brugia malayi on the growth and proliferation of endothelial cells in vitro. Journal of Parasitology 82, 550–556.Google Scholar
Ratra, D., Phogat, C., Singh, M. and Choudhari, N. S. (2010). Intravitreal cysticercosis presenting as neovascular glaucoma. Indian Journal of Ophthalmology 58, 70–73.Google Scholar
Restrepo, B. I., Alvarez, J. I., Castano, J. A., Arias, L. F., Restrepo, M., Trujillo, J., Colegial, C. H. and Teale, J. M. (2001). Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infection and Immunity 69, 4554–4560.Google Scholar
Ritter, D. M. and McKerrow, J. H. (1996). Intercellular adhesion molecule 1 is the major adhesion molecule expressed during schistosome granuloma formation. Infection and Immunity 64, 4706–4713.Google Scholar
Rodriguez-Manzaneque, J. C., Lane, T. F., Ortega, M. A., Hynes, R. O., Lawler, J. and Iruela-Arispe, M. L. (2001). Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proceedings of the National Academy of Sciences, USA 98, 12485–12490.Google Scholar
Ross, R. (1986). The pathogenesis of atherosclerosis – an update. New England Journal of Medicine 314, 488–500.Google Scholar
Shariati, F., Perez-Arellano, J. L., Lopez-Aban, J., Arefi, M., Martinez-Fernandez, A. R. and Muro, A. (2009). Trichinella: differential expression of angiogenic factors in macrophages stimulated with antigens from encapsulated and non-encapsulated species. Experimental Parasitology 123, 347–353.Google Scholar
Shariati, F., Perez-Arellano, J. L., Lopez-Aban, J., El Behairy, A. M. and Muro, A. (2010). Role of angiogenic factors in acute experimental Strongyloides venezuelensis infection. Parasite Immunology 32, 430–439.Google Scholar
Shibuya, M. (2006). Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. Journal of Biochemistry and Molecular Biology 39, 469–478.Google Scholar
Shibuya, M. (2008). Vascular endothelial growth factor-dependent and -independent regulation of angiogenesis. BMB Reports 41, 278–286.CrossRefGoogle ScholarPubMed
Shirai, W., Sato, T., Shibuya, H., Naito, K. and Tsukise, A. (2006). Anatomicopathological study of vascular and biliary systems using cast samples of Fasciola-infected bovine livers. Journal of Veterinary Medicine A 53, 239–245.Google Scholar
Sikasunge, C. S., Johansen, M. V., Phiri, I. K., Willingham, A. L. 3rd and Leifsson, P. S. (2009). The immune response in Taenia solium neurocysticercosis in pigs is associated with astrogliosis, axonal degeneration and altered blood-brain barrier permeability. Veterinary Parasitology 160, 242–250.Google Scholar
Silva, L. M., Ribeiro-Dos-Santos, R., Soares, M. B. and Andrade, Z. A. (2006). Characterization of the vascular changes in schistosomal portal (pipestem) fibrosis of mice. Acta Tropica 98, 34–42.Google Scholar
Simon, F., Morchon, R., Rodriguez-Barbero, A., Lopez-Belmonte, J., Grandi, G. and Genchi, C. (2008). Dirofilaria immitis and Wolbachia-derived antigens: its effect on endothelial mammal cells. Veterinary Parasitology 158, 223–231.Google Scholar
Singh, K. P., Gerard, H. C., Hudson, A. P. and Boros, D. L. (2004). Expression of matrix metalloproteinases and their inhibitors during the resorption of schistosome egg-induced fibrosis in praziquantel-treated mice. Immunology 111, 343–352.Google Scholar
Smith, R. J., Cotter, T. P., Williams, J. F. and Guderian, R. H. (1988). Vascular perfusion of Onchocerca volvulus nodules. Tropical Medicine and Parasitology 39, 418–421.Google Scholar
Smout, M. J., Laha, T., Mulvenna, J., Sripa, B., Suttiprapa, S., Jones, A., Brindley, P. J. and Loukas, A. (2009). A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathogens 5, e1000611.Google Scholar
Sripa, B., Bethony, J. M., Sithithaworn, P., Kaewkes, S., Mairiang, E., Loukas, A., Mulvenna, J., Laha, T., Hotez, P. J. and Brindley, P. J. (2010). Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Tropica doi:10.1016/j.actatropica.2010.07.006Google Scholar
Sripa, B., Kaewkes, S., Sithithaworn, P., Mairiang, E., Laha, T., Smout, M., Pairojkul, C., Bhudhisawasdi, V., Tesana, S., Thinkamrop, B., Bethony, J. M., Loukas, A. and Brindley, P. J. (2007). Liver fluke induces cholangiocarcinoma. PLoS Medicine 4, e201.Google Scholar
Stadelmann, B., Spiliotis, M., Muller, J., Scholl, S., Muller, N., Gottstein, B. and Hemphill, A. (2010). Echinococcus multilocularis phosphoglucose isomerase (EmPGI): A glycolytic enzyme involved in metacestode growth and parasite-host cell interactions. International Journal for Parasitology 40, 1563–1574.Google Scholar
Stockdale, P. H. G. (1970). The pathogenesis of the lesions elicited by Aelurostrongylus abstrusus during its prepatent period. Pathologia Veterinaria 7, 102–115.Google Scholar
Tarsitano, M., De Falco, S., Colonna, V., McGhee, J. D. and Persico, M. G. (2006). The C. elegans pvf-1 gene encodes a PDGF/VEGF-like factor able to bind mammalian VEGF receptors and to induce angiogenesis. The FASEB Journal 20, 227–233.Google Scholar
Tawe, W., Pearlman, E., Unnasch, T. R. and Lustigman, S. (2000). Angiogenic activity of Onchocerca volvulus recombinant proteins similar to vespid venom antigen 5. Molecular and Biochemical Parasitology 109, 91–99.Google Scholar
Tawfeek, G. M., Alafifi, A. M. and Azmy, M. F. (2003). Immunological indicators of morbidity in human schistosomiasis mansoni: role of vascular endothelial growth factor and anti-soluble egg antigen IgG4 in disease progression. Journal of the Egyptian Society of Parasitology 33, 597–614.Google Scholar
Trottein, F., Descamps, L., Nutten, S., Dehouck, M. P., Angeli, V., Capron, A., Cecchelli, R. and Capron, M. (1999). Schistosoma mansoni activates host microvascular endothelial cells to acquire an anti-inflammatory phenotype. Infection and Immunity 67, 3403–3409.Google Scholar
Tsai, H. C., Chung, L. Y., Chen, E. R., Liu, Y. C., Lee, S. S., Chen, Y. S., Sy, C. L., Wann, S. R. and Yen, C. M. (2008). Association of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinase-4 in cerebrospinal fluid with blood-brain barrier dysfunction in patients with eosinophilic meningitis caused by Angiostrongylus cantonensis. American Journal of Tropical Medicine and Hygiene 78, 20–27.Google Scholar
Tsai, H. C., Huang, Y. L., Liu, Y. C., Wann, S. R., Lee, S. S., Chen, E. R., Yen, C. M., Tai, M. H., Shi, M. H. and Chen, Y. S. (2009). Dynamic changes of hepatocyte growth factor in eosinophilic meningitis caused by Angiostrongylus cantonensis infection. American Journal of Tropical Medicine and Hygiene 80, 980–982.Google Scholar
Tsai, H. C., Liu, Y. C., Lee, S. S., Chen, E. R. and Yen, C. M. (2007). Vascular endothelial growth factor is associated with blood brain barrier dysfunction in eosinophilic meningitis caused by Angiostrongylus cantonensis infection. American Journal of Tropical Medicine and Hygiene 76, 592–595.Google Scholar
Uchide, T. and Saida, K. (2005). Elevated endothelin-1 expression in dogs with heartworm disease. Journal of Veterinary Medical Science 67, 1155–1161.Google Scholar
Vaillant, B., Chiaramonte, M. G., Cheever, A. W., Soloway, P. D. and Wynn, T. A. (2001). Regulation of hepatic fibrosis and extracellular matrix genes by the th response: new insight into the role of tissue inhibitors of matrix metalloproteinases. Journal of Immunology 167, 7017–7026.CrossRefGoogle Scholar
Van der Merwe, L. L., Kirberger, R. M., Clift, S., Williams, M., Keller, N. and Naidoo, V. (2008). Spirocerca lupi infection in the dog: a review. The Veterinary Journal 176, 294–309.Google Scholar
Van de Vijver, K. K., Colpaert, C. G., Jacobs, W., Kuypers, K., Hokke, C. H., Deelder, A. M. and Van Marck, E. A. (2006). The host's genetic background determines the extent of angiogenesis induced by schistosome egg antigens. Acta Tropica 99, 243–251.Google Scholar
Van Hinsbergh, V. W. and Koolwijk, P. (2008). Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovascular Research 78, 203–212.Google Scholar
Venco, L. (2007). Heartworm (Dirofilaria immitis) disease in dogs. In Dirofilaria immitis and D. repens in Dog and Cat and Human Infections (ed. Genchi, C., Rinaldi, L. and Cringoli, G.), Mappe Parassitologiche 8, 117–125.Google Scholar
Volkmann, L., Fischer, K., Taylor, M. and Hoerauf, A. (2003). Antibiotic therapy in murine filariasis (Litomosoides sigmodontis): comparative effects of doxycycline and rifampicin on Wolbachia and filarial viability. Tropical Medicine and International Health 8, 392–401.Google Scholar
Wang, Q. P., Lai, D. H., Zhu, X. Q., Chen, X. G. and Lun, Z. R. (2008). Human angiostrongyliasis. The Lancet Infectious Diseases 8, 621–630.Google Scholar
Weina, P. J. and Burns, W. C. (1992). Mortality in Syrian hamsters infected with Paragonimus kellicotti. Journal of Parasitology 78, 378–380.Google Scholar
Weina, P. J. and England, D. M. (1990). The American lung fluke, Paragonimus kellicotti, in a cat model. Journal of Parasitology 76, 568–572.Google Scholar
Weiss, A. T., Bauer, C. and Kohler, K. (2010). Canine alveolar echinococcosis: morphology and inflammatory response. Journal of Comparative Pathology (in the Press), 143, 233–238.CrossRefGoogle ScholarPubMed
Wyler, D. J. (1996). Fibrosin, a novel fibrogenic protein: discovery, cloning and implications for fibrotic disorders. International Archives of Allergy and Immunology 111, 326–329.Google Scholar
Wyler, D. J., Prakash, S. and Libby, P. (1987). Mesenchymal target cell specificity of egg granuloma-derived fibroblast growth factor in schistosomiasis. Journal of Infectious Diseases 155, 728–736.Google Scholar
Wyler, D. J. and Tracy, J. W. (1982). Direct and indirect effects of soluble extracts of Schistosoma mansoni eggs on fibroblast proliferation in vitro. Infection and Immunity 38, 103–108.Google Scholar
Yancopoulos, G. D., Davis, S., Gale, N. W., Rudge, J. S., Wiegand, S. J. and Holash, J. (2000). Vascular-specific growth factors and blood vessel formation. Nature, London 407 (6801), 242–248.Google Scholar
Yoshimura, K., Aiba, H., Oya, H. and Fukuda, Y. (1980). Angiostrongylus cantonensis: development following pulmonary arterial transfers into permissive and nonpermissive hosts. Experimental Parasitology 49, 339–352.Google Scholar
Young, N. D., Campbell, B. E., Hall, R. S., Jex, A. R., Cantacessi, C., Laha, T., Sohn, W. M., Sripa, B., Loukas, A., Brindley, P. J. and Gasser, R. B. (2010). Unlocking the transcriptomes of two carcinogenic parasites, Clonorchis sinensis and Opisthorchis viverrini. PLoS Neglected Tropical Diseases 4, e719.Google Scholar