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Angiogenesis in cardiopulmonary dirofilariosis: does the Wolbachia surface protein have a pro- or anti-angiogenic effect?

Published online by Cambridge University Press:  10 June 2020

T. Zueva ,
R. Morchón Open the ORCID record for R. Morchón [Opens in a new window] ,
E. Carretón ,
C. Ollauri-Ibáñez ,
M. Pericacho ,
A. Rodríguez-Barbero  and
F. Simón Open the ORCID record for F. Simón [Opens in a new window]
T. Zueva
Affiliation:
Group of Animal and Human Dirofilariosis, Parasitology Area, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, Salamanca37007, Spain
R. Morchón
Affiliation:
Group of Animal and Human Dirofilariosis, Parasitology Area, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, Salamanca37007, Spain
E. Carretón
Affiliation:
Faculty of Veterinary Medicine, Research Institute of Biomedical and Health Sciences (IUIBS), University of Las Palmas de Gran Canaria, Trasmontaña s/n, Arucas, 35413Las Palmas, Spain
C. Ollauri-Ibáñez
Affiliation:
Department of Physiology and Pharmacology, Biomedical Research Institute of Salamanca (IBSAL), University of Salamanca, Salamanca, Spain
M. Pericacho
Affiliation:
Department of Physiology and Pharmacology, Biomedical Research Institute of Salamanca (IBSAL), University of Salamanca, Salamanca, Spain
A. Rodríguez-Barbero
Affiliation:
Department of Physiology and Pharmacology, Biomedical Research Institute of Salamanca (IBSAL), University of Salamanca, Salamanca, Spain
F. Simón*
Affiliation:
Group of Animal and Human Dirofilariosis, Parasitology Area, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, Salamanca37007, Spain
*
Author for correspondence: F. Simón, E-mail: fersimon@usal.es
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Abstract

Cardiopulmonary dirofilariosis caused by Dirofilaria immitis produces inflammation, blood vessel obstruction and hypoxia, which are required conditions for the beginning of the process of neovascularization. Since D. immitis harbours intracellular symbiotic Wolbachia bacterium, the global understanding of the angiogenic process requires the analysis of the effect of the parasite molecules, but also that of Wolbachia. Canine primary lung microvascular endothelial cells were treated with the recombinant Wolbachia surface protein (rWSP) and the expression of angiogenic factors like Vascular Endothelial Growth Factor-A (VEGF-A), sFlt, membrane Endoglin (mEndoglin) and soluble Endoglin (sEndoglin), as well as the in vitro formation of pseudocapillaries, were measured. The analyses showed a significant increase in the expression of pro-angiogenic VEGF-A and anti-angiogenic sEndoglin, together with a significant decrease in both pro-angiogenic mEndoglin and pseudocapillary formation, compared to untreated controls. Due to the complexity of the angiogenic process and its relationship with other physiological processes like inflammation and fibrinolysis, these results might suggest that rWSP participate in various mechanisms related to each other and its effects might depend either on the balance between them or on the moment of their occurrence.

Keywords

Wolbachiaangiogenesiscardiopulmonary dirofilariosisvascular endothelial cells
Type
Short Communication
Information
Journal of Helminthology , Volume 94 , 2020 , e162
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Adams, RH and Alitalo, K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nature Reviews Molecular Cell Biology 8, 464–478.CrossRefGoogle ScholarPubMed
Alitalo, K and Carmeliet, P (2002) Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 1, 219–227.CrossRefGoogle ScholarPubMed
Bennuru, S and Nutman, TB (2009) Lymphatics in human lymphatic filariasis: in vitro models of parasite-induced lymphatic remodeling. Lymphatic Research and Biology 7, 215–219.CrossRefGoogle ScholarPubMed
Brattig, NW, Bazzocchi, C, Kirsching, CJ, et al. (2004) The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune response through TLR2 and TLR4. Journal of Immunology 73, 437–445.CrossRefGoogle Scholar
Dennis, RD, Schubert, U and Bauer, C (2011) Angiogenesis and parasitic helminth-associated neovascularization. Parasitology 138, 426–439.CrossRefGoogle ScholarPubMed
Diosdado, A, Gómez, PJ, Morchón, R, Simón, F and González-Miguel, J (2017) Interaction between Wolbachia and the fibrinolytic system as a possible pathological mechanism in cardiopulmonary dirofilariosis. Veterinary Parasitology 247, 64–69.CrossRefGoogle ScholarPubMed
Figueroa, AL, Subramanian, SS, Cury, RC, Truong, QA, Gardecki, JA, Tearney, GJ, Hoffmann, U, Brady, TJ and Tawakol, A (2012) Distribution of inflammation within carotid atherosclerotic plaques with high-risk morphological features: a comparison between positron emission tomography activity, plaque morphology, and histopathology. Circulation: Cardiovascular Imaging 5, 69–77.Google ScholarPubMed
González-Miguel, J, Morchón, R, Mellado, I, Carretón, E, Montoya-Alonso, JA and Simón, F (2012) Excretory/secretory antigens from Dirofilaria immitis adult worms interact with the host fibrinolytic system involving the vascular endothelium. Molecular and Biochemical Parasitology 181, 134–140.CrossRefGoogle ScholarPubMed
González-Miguel, J, Morchón, R, Carretón, E, Montoya-Alonso, JA and Simón, F (2013) Surface associated antigens of Dirofilaria immitis adult worms activate the host fibrinolytic system. Veterinary Parasitology 196, 235–240.CrossRefGoogle ScholarPubMed
González-Miguel, J, Morchón, R, Siles-Lucas, M and Simón, F (2015) Fibrinolysis and proliferative endarteritis: two related processes in chronic infections? The model of the blood-borne pathogen Dirofilaria immitis. PLoS One 10, e012445.CrossRefGoogle ScholarPubMed
González-Miguel, J, Siles-Lucas, M, Kartashev, V, Morchón, R and Simón, F (2016) Plasmin in parasitic chronic infections: friend or foe? Trends in Parasitology 32, 325–335.CrossRefGoogle ScholarPubMed
Hormaeche, M, Carretón, E, González-Miguel, J, Gussoni, S, Montoya-Alonso, JA, Simón, F and Morchón, R (2014) Proteomic analysis of the urine of Dirofilaria immitis infected dogs. Veterinary Parasitology 203, 241–246.CrossRefGoogle ScholarPubMed
Jerckic, M, Rivas-Elena, JV, Santibáñez, JF, et al. (2006) Endoglin regulates cyclooxygenase-2 expression and activity. Circulation Research 99, 248–256.CrossRefGoogle Scholar
Kramer, L, Simón, F, Tamarozzi, F, Genchi, M and Bazzocchi, C (2005) Is Wolbachia complicating the pathological effects of Dirofilaria immitis infections? Veterinary Parasitology 133, 133–136.CrossRefGoogle ScholarPubMed
Morchón, R, Bazzocchi, C, López-Belmonte, J, Martín-Pacho, JR, Kramer, LH, Grandi, G and Simón, F (2007) iNOs expression is stimulated by the major surface protein (rWSP) from Wolbachia bacterial endosymbiont of Dirofilaria immitis following subcutaneous injection in mice. Parasitology International 56, 71–75.CrossRefGoogle ScholarPubMed
Narimatsu, A, Hattori, T, Koike, N, et al. (2019) Corneal lymphangiogenesis ameliorates corneal inflammation and edema in late stage of bacterial keratitis. Scientific Reports 9, 2984.CrossRefGoogle ScholarPubMed
Núñez-Gómez, E, Pericacho, M, Ollauri-Ibanez, C, Bernabeu, C and Lopez-Novoa, JM (2017) The role of endoglin in post-ischemic revascularization. Angiogenesis 20, 1–24.CrossRefGoogle ScholarPubMed
Sironi, M, Bandi, C, Sacchi, L, Di Sacco, B, Damiani, G and Genchi, C (1995) Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm. Molecular and Biochemical Parasitology 74, 223–227.CrossRefGoogle Scholar
Tawe, W, Pearlman, E, Unnasch, TR and Lustigman, S (2000) Angiogenic activity of Onchocerca volvulus recombinant proteins similar to vespid venom antigen 5. Molecular and Biochemical Parasitology 109, 91–99.CrossRefGoogle ScholarPubMed
Taylor, MJ, Cross, HF, Ford, L, Makunde, WH, Prasad, GB and Bilo, K (2001) Wolbachia bacteria in filarial immunity and disease. Parasite Immunology 23, 401–409.CrossRefGoogle ScholarPubMed
Urbanowicz, M, Kutzner, H, Riveiro-Falkenbach, E and Rodriguez-Peralto, JL (2016) Infectious angiogenesis-different pathways, the same goal. The American Journal of Dermatopathology 38, 793–801.CrossRefGoogle ScholarPubMed
Zueva, T, Morchón, R, Carretón, E, Montoya-Alonso, JA, Santana, A, Bargues, MD, Mas-Coma, S, Rodríguez-Barbero, A and Simón, F (2019) Angiogenic response in an in vitro model of dog microvascular endothelial cells stimulated with antigenic extracts from Dirofilaria immitis adult worms. Parasite & Vectors 12, 315.CrossRefGoogle Scholar