The Role of Snake Venom Disintegrins in Angiogenesis
Abstract
1. Introduction
1.1. Angiogenesis
1.2. Integrins
1.3. Snake Venom Metalloproteinases and Snake Venom Disintegrins
1.4. The Role and Properties of SVDs in Angiogenesis
Interference of SVD with VEGF
1.5. Anti-Angiogenic Effects of SVDs
2. Potential Applications of SVD in Angiogenesis-Related Diseases
2.1. Cancer
2.2. Ocular Diseases, e.g., Diabetic Retinopathy
3. Utilization of SVD as Pro-Angiogenic Agents
3.1. Tissue Regeneration and Wound Healing
3.2. Cardiovascular Diseases
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Carmeliet, P.; Jain, R.K. Angiogenesis in cancer and other diseases. Nature 2000, 407, 249–257. [Google Scholar] [CrossRef]
- Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1995, 1, 27–31. [Google Scholar] [CrossRef] [PubMed]
- Potente, M.; Gerhardt, H.; Carmeliet, P. Basic and therapeutic aspects of angiogenesis. Cell 2011, 146, 873–887. [Google Scholar] [CrossRef] [PubMed]
- Matsumoto, T.; Claesson-Welsh, L. VEGF receptor signal transduction. Sci. STKE 2001, 2001, re21. [Google Scholar] [CrossRef] [PubMed]
- Zhang, F.; Tang, Z.; Hou, X.; Lennartsson, J.; Li, Y.; Koch, A.W.; Scotney, P.; Lee, C.; Arjunan, P.; Dong, L.; et al. VEGF-B is dispensable for blood vessel growth but critical for their survival, and VEGF-B targeting inhibits pathological angiogenesis. Proc. Natl. Acad. Sci. USA 2009, 106, 6152–6157. [Google Scholar] [CrossRef] [PubMed]
- Dvorak, H.F. Vascular permeability factor/vascular endothelial growth factor: A critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 2002, 20, 4368–4380. [Google Scholar] [CrossRef] [PubMed]
- Swenson, S.; Ramu, S.; Markland, F.S. Anti-angiogenesis and RGD-containing snake venom disintegrins. Curr. Pharm. Des. 2007, 13, 2860–2871. [Google Scholar] [CrossRef] [PubMed]
- Usami, Y.; Fujimura, Y.; Miura, S.; Shima, H.; Yoshida, E.; Yoshioka, A.; Hirano, K.; Suzuki, M.; Titani, K. A 28 kDa-protein with disintegrin-like structure (jararhagin-C) purified from Bothrops jararaca venom inhibits collagen- and ADP-induced platelet aggregation. Biochem. Biophys. Res. Commun. 1994, 201, 331–339. [Google Scholar] [CrossRef]
- Takada, Y.; Ye, X.; Simon, S. The integrins. Genome Biol. 2007, 8, 215. [Google Scholar] [CrossRef]
- Rose, D.M.; Alon, R.; Ginsberg, M.H. Integrin modulation and signaling in leukocyte adhesion and migration. Immunol. Rev. 2007, 218, 126–134. [Google Scholar] [CrossRef]
- Hynes, R.O. Integrins: Bidirectional, allosteric signaling machines. Cell 2002, 110, 673–687. [Google Scholar] [CrossRef] [PubMed]
- Ruoslahti, E.; Pierschbacher, M.D. New perspectives in cell adhesion: RGD and integrins. Science 1987, 238, 491–497. [Google Scholar] [CrossRef] [PubMed]
- Lu, X.; Lu, D.; Scully, M.F.; Kakkar, V.V. Integrins in drug targeting-RGD templates in toxins. Curr. Pharm. Des. 2006, 12, 2749–2769. [Google Scholar] [CrossRef] [PubMed]
- Marcinkiewicz, C.; Vijay-Kumar, S.; McLane, M.A.; Niewiarowski, S. Significance of RGD loop and C-terminal domain of echistatin for recognition of αIIbβ3 and αvβ3 integrins and expression of ligand-induced binding site. Blood 1997, 90, 1565–1575. [Google Scholar] [CrossRef] [PubMed]
- Kamata, T.; Handa, M.; Sato, Y.; Ikeda, Y.; Aiso, S. Membrane-proximal α/βstalk interactions differentially regulate integrin activation. J. Biol. Chem. 2005, 280, 24775–24783. [Google Scholar] [CrossRef] [PubMed]
- Calvete, J.J. Snake venomics: From the inventory of toxins to biology. Toxicon 2013, 75, 44–62. [Google Scholar] [CrossRef] [PubMed]
- Arruda Macedo, J.K.; Fox, J.W.; de Souza Castro, M. Disintegrins from snake venoms and their applications in cancer research and therapy. Curr. Protein Pept. Sci. 2015, 16, 532–548. [Google Scholar] [CrossRef]
- Marcinkiewicz, C. Applications of snake venom components to modulate integrin activities in cell-matrix interactions. Int. J. Biochem. Cell Biol. 2013, 45, 1974–1986. [Google Scholar] [CrossRef]
- Tasoulis, T.; Isbister, G.K. A Review and Database of Snake Venom Proteomes. Toxins 2017, 9, 290. [Google Scholar] [CrossRef]
- Fox, J.W.; Serrano, S.M. Timeline of key events in snake venom metalloproteinase research. J. Proteom. 2009, 72, 200–209. [Google Scholar] [CrossRef]
- Fox, J.W.; Serrano, S.M. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J. 2008, 275, 3016–3030. [Google Scholar] [CrossRef]
- Calvete, J.J.; Marcinkiewicz, C.; Monleon, D.; Esteve, V.; Celda, B.; Juarez, P.; Sanz, L. Snake venom disintegrins: Evolution of structure and function. Toxicon 2005, 45, 1063–1074. [Google Scholar] [CrossRef]
- Schonthal, A.H.; Swenson, S.D.; Chen, T.C.; Markland, F.S. Preclinical studies of a novel snake venom-derived recombinant disintegrin with antitumor activity: A review. Biochem. Pharmacol. 2020, 181, 114149. [Google Scholar] [CrossRef] [PubMed]
- Calvete, J.J.; Moreno-Murciano, M.P.; Theakston, R.D.; Kisiel, D.G.; Marcinkiewicz, C. Snake venom disintegrins: Novel dimeric disintegrins and structural diversification by disulphide bond engineering. Biochem. J. 2003, 372, 725–734. [Google Scholar] [CrossRef] [PubMed]
- Marcinkiewicz, C. Functional characteristic of snake venom disintegrins: Potential therapeutic implication. Curr. Pharm. Des. 2005, 11, 815–827. [Google Scholar] [CrossRef] [PubMed]
- Clissa, P.B.; Lopes-Ferreira, M.; Della-Casa, M.S.; Farsky, S.H.; Moura-da-Silva, A.M. Importance of jararhagin disintegrin-like and cysteine-rich domains in the early events of local inflammatory response. Toxicon 2006, 47, 591–596. [Google Scholar] [CrossRef] [PubMed]
- Zychar, B.C.; Clissa, P.B.; Carvalho, E.; Baldo, C.; Goncalves, L.R.C. Leukocyte recruitment induced by snake venom metalloproteinases: Role of the catalytic domain. Biochem. Biophys. Res. Commun. 2020, 521, 402–407. [Google Scholar] [CrossRef]
- Zychar, B.C.; Clissa, P.B.; Carvalho, E.; Alves, A.S.; Baldo, C.; Faquim-Mauro, E.L.; Goncalves, L.R.C. Modulation of Adhesion Molecules Expression by Different Metalloproteases Isolated from Bothrops Snakes. Toxins 2021, 13, 803. [Google Scholar] [CrossRef]
- Souza, D.H.; Iemma, M.R.; Ferreira, L.L.; Faria, J.P.; Oliva, M.L.; Zingali, R.B.; Niewiarowski, S.; Selistre-de-Araujo, H.S. The disintegrin-like domain of the snake venom metalloprotease alternagin inhibits α2β1 integrin-mediated cell adhesion. Arch. Biochem. Biophys. 2000, 384, 341–350. [Google Scholar] [CrossRef]
- Mebs, D. Myotoxic activity of phospholipases A2 isolated from cobra venoms: Neutralization by polyvalent antivenoms. Toxicon 1986, 24, 1001–1008. [Google Scholar] [CrossRef]
- Della-Casa, M.S.; Junqueira-de-Azevedo, I.; Butera, D.; Clissa, P.B.; Lopes, D.S.; Serrano, S.M.; Pimenta, D.C.; Magalhaes, G.S.; Ho, P.L.; Moura-da-Silva, A.M. Insularin, a disintegrin from Bothrops insularis venom: Inhibition of platelet aggregation and endothelial cell adhesion by the native and recombinant GST-insularin proteins. Toxicon 2011, 57, 125–133. [Google Scholar] [CrossRef] [PubMed]
- Gan, Z.R.; Gould, R.J.; Jacobs, J.W.; Friedman, P.A.; Polokoff, M.A. Echistatin. A potent platelet aggregation inhibitor from the venom of the viper, Echis carinatus. J. Biol. Chem. 1988, 263, 19827–19832. [Google Scholar] [CrossRef] [PubMed]
- Kamiguti, A.S.; Zuzel, M.; Theakston, R.D. Snake venom metalloproteinases and disintegrins: Interactions with cells. Braz. J. Med. Biol. Res. 1998, 31, 853–862. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.H.; Yang, R.S.; Liu, C.Z.; Huang, T.F.; Fu, W.M. Differential susceptibility of osteosarcoma cells and primary osteoblasts to cell detachment caused by snake venom metalloproteinase protein. Toxicon 2004, 43, 11–20. [Google Scholar] [CrossRef] [PubMed]
- Brooks, S.A.; Lomax-Browne, H.J.; Carter, T.M.; Kinch, C.E.; Hall, D.M. Molecular interactions in cancer cell metastasis. Acta Histochem. 2010, 112, 3–25. [Google Scholar] [CrossRef] [PubMed]
- Desgrosellier, J.S.; Cheresh, D.A. Integrins in cancer: Biological implications and therapeutic opportunities. Nat. Rev. Cancer 2010, 10, 9–22. [Google Scholar] [CrossRef] [PubMed]
- Golubkov, V.; Hawes, D.; Markland, F.S. Anti-angiogenic activity of contortrostatin, a disintegrin from Agkistrodon contortrix contortrix snake venom. Angiogenesis 2003, 6, 213–224. [Google Scholar] [CrossRef]
- Maiguel, D.; Faridi, M.H.; Wei, C.; Kuwano, Y.; Balla, K.M.; Hernandez, D.; Barth, C.J.; Lugo, G.; Donnelly, M.; Nayer, A.; et al. Small molecule-mediated activation of the integrin CD11b/CD18 reduces inflammatory disease. Sci. Signal. 2011, 4, ra57. [Google Scholar] [CrossRef]
- Petpiroon, N.; Sritularak, B.; Chanvorachote, P. Correction: Phoyunnanin E inhibits migration of non-small cell lung cancer cells via suppression of epithelial-to-mesenchymal transition and integrin αv and integrin β3. BMC Complement. Med. Ther. 2023, 23, 196. [Google Scholar] [CrossRef]
- Jahangiri, A.; Aghi, M.K.; Carbonell, W.S. β1 integrin: Critical path to antiangiogenic therapy resistance and beyond. Cancer Res. 2014, 74, 3–7. [Google Scholar] [CrossRef]
- Liu, F.; Wu, Q.; Dong, Z.; Liu, K. Integrins in cancer: Emerging mechanisms and therapeutic opportunities. Pharmacol. Ther. 2023, 247, 108458. [Google Scholar] [CrossRef] [PubMed]
- Olfa, K.Z.; Jose, L.; Salma, D.; Amine, B.; Najet, S.A.; Nicolas, A.; Maxime, L.; Raoudha, Z.; Kamel, M.; Jacques, M.; et al. Lebestatin, a disintegrin from Macrovipera venom, inhibits integrin-mediated cell adhesion, migration and angiogenesis. Lab. Investig. 2005, 85, 1507–1516. [Google Scholar] [CrossRef]
- Yeh, C.H.; Peng, H.C.; Huang, T.F. Accutin, a new disintegrin, inhibits angiogenesis in vitro and in vivo by acting as integrin αvβ3 antagonist and inducing apoptosis. Blood 1998, 92, 3268–3276. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, B.A.; De Moura, F.B.R.; Tomiosso, T.C.; Correa, N.C.R.; Goulart, L.R.; Barcelos, L.S.; Clissa, P.B.; Araujo, F.A. Jararhagin-C, a disintegrin-like protein, improves wound healing in mice through stimulation of M2-like macrophage, angiogenesis and collagen deposition. Int. Immunopharmacol. 2021, 101, 108224. [Google Scholar] [CrossRef]
- Monteiro, D.A.; Kalinin, A.L.; Selistre-de-Araujo, H.S.; Nogueira, L.A.N.; Beletti, M.E.; Fernandes, M.N.; Rantin, F.T. Cardioprotective effects of alternagin-C (ALT-C), a disintegrin-like protein from Rhinocerophis alternatus snake venom, on hypoxia-reoxygenation-induced injury in fish. Comp. Biochem. Physiology. Toxicol. Pharmacol. 2019, 215, 67–75. [Google Scholar] [CrossRef]
- Marcinkiewicz, C.; Weinreb, P.H.; Calvete, J.J.; Kisiel, D.G.; Mousa, S.A.; Tuszynski, G.P.; Lobb, R.R. Obtustatin: A potent selective inhibitor of α1β1 integrin in vitro and angiogenesis in vivo. Cancer Res. 2003, 63, 2020–2023. [Google Scholar]
- Staniszewska, I.; Walsh, E.M.; Rothman, V.L.; Gaathon, A.; Tuszynski, G.P.; Calvete, J.J.; Lazarovici, P.; Marcinkiewicz, C. Effect of VP12 and viperistatin on inhibition of collagen-receptor-dependent melanoma metastasis. Cancer Biol. Ther. 2009, 8, 1507–1516. [Google Scholar] [CrossRef] [PubMed]
- Sanz, L.; Chen, R.Q.; Perez, A.; Hilario, R.; Juarez, P.; Marcinkiewicz, C.; Monleon, D.; Celda, B.; Xiong, Y.L.; Perez-Paya, E.; et al. cDNA cloning and functional expression of jerdostatin, a novel RTS-disintegrin from Trimeresurus jerdonii and a specific antagonist of the α1β1 integrin. J. Biol. Chem. 2005, 280, 40714–40722. [Google Scholar] [CrossRef]
- Yeh, C.H.; Peng, H.C.; Yang, R.S.; Huang, T.F. Rhodostomin, a snake venom disintegrin, inhibits angiogenesis elicited by basic fibroblast growth factor and suppresses tumor growth by a selective αvβ3 blockade of endothelial cells. Mol. Pharmacol. 2001, 59, 1333–1342. [Google Scholar] [CrossRef]
- Dos Santos, P.K.; Altei, W.F.; Danilucci, T.M.; Lino, R.L.B.; Pachane, B.C.; Nunes, A.C.C.; Selistre-de-Araujo, H.S. Alternagin-C (ALT-C), a disintegrin-like protein, attenuates α2β1 integrin and VEGF receptor 2 signaling resulting in angiogenesis inhibition. Biochimie 2020, 174, 144–158. [Google Scholar] [CrossRef]
- Selistre-de-Araujo, H.S.; Cominetti, M.R.; Terruggi, C.H.; Mariano-Oliveira, A.; De Freitas, M.S.; Crepin, M.; Figueiredo, C.C.; Morandi, V. Alternagin-C, a disintegrin-like protein from the venom of Bothrops alternatus, modulates α2β1 integrin-mediated cell adhesion, migration and proliferation. Braz. J. Med. Biol. Res. 2005, 38, 1505–1511. [Google Scholar] [CrossRef] [PubMed]
- Limam, I.; Abdelkarim, M.; El Ayeb, M.; Crepin, M.; Marrakchi, N.; Di Benedetto, M. Disintegrin-like Protein Strategy to Inhibit Aggressive Triple-Negative Breast Cancer. Int. J. Mol. Sci. 2023, 24, 12219. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Q.; Nakada, M.T.; Arnold, C.; Shieh, K.Y.; Markland, F.S., Jr. Contortrostatin, a dimeric disintegrin from Agkistrodon contortrix contortrix, inhibits angiogenesis. Angiogenesis 1999, 3, 259–269. [Google Scholar] [CrossRef] [PubMed]
- Ramos, O.H.; Kauskot, A.; Cominetti, M.R.; Bechyne, I.; Salla Pontes, C.L.; Chareyre, F.; Manent, J.; Vassy, R.; Giovannini, M.; Legrand, C.; et al. A novel αvβ3-blocking disintegrin containing the RGD motive, DisBa-01, inhibits bFGF-induced angiogenesis and melanoma metastasis. Clin. Exp. Metastasis 2008, 25, 53–64. [Google Scholar] [CrossRef] [PubMed]
- Chang, C.H.; Chung, C.H.; Hsu, C.C.; Peng, H.C.; Huang, T.F. Inhibitory effects of polypeptides derived from a snake venom C-type lectin, aggretin, on tumor cell-induced platelet aggregation. J. Thromb. Haemost. 2014, 12, 540–549. [Google Scholar] [CrossRef] [PubMed]
- Huang, T.F.; Ouyang, C. Action mechanism of the potent platelet aggregation inhibitor from Trimeresurus gramineus snake venom. Thromb. Res. 1984, 33, 125–138. [Google Scholar] [CrossRef]
- Ren, A.; Wang, S.; Cai, W.; Yang, G.; Zhu, Y.; Wu, X.; Zhang, Y. Agkistin-s, a disintegrin domain, inhibits angiogenesis and induces BAECs apoptosis. J. Cell. Biochem. 2006, 99, 1517–1523. [Google Scholar] [CrossRef]
- Takahashi, H.; Hattori, S.; Iwamatsu, A.; Takizawa, H.; Shibuya, M. A novel snake venom vascular endothelial growth factor (VEGF) predominantly induces vascular permeability through preferential signaling via VEGF receptor-1. J. Biol. Chem. 2004, 279, 46304–46314. [Google Scholar] [CrossRef]
- Yamazaki, Y.; Matsunaga, Y.; Tokunaga, Y.; Obayashi, S.; Saito, M.; Morita, T. Snake venom Vascular Endothelial Growth Factors (VEGF-Fs) exclusively vary their structures and functions among species. J. Biol. Chem. 2009, 284, 9885–9891. [Google Scholar] [CrossRef]
- Ferrara, N. VEGF-A: A critical regulator of blood vessel growth. Eur. Cytokine Netw. 2009, 20, 158–163. [Google Scholar] [CrossRef]
- Chakrabarty, D.; Chanda, C. Snake Venom Disintegrins. In Snake Venoms; Inagaki, H., Vogel, C.-W., Mukherjee, A.K., Rahmy, T.R., Gopalakrishnakone, P., Eds.; Springer: Dordrecht, The Netherlands, 2017; pp. 437–449. [Google Scholar]
- Swenson, S.; Costa, F.; Ernst, W.; Fujii, G.; Markland, F.S. Contortrostatin, a snake venom disintegrin with anti-angiogenic and anti-tumor activity. Pathophysiol. Haemost. Thromb. 2005, 34, 169–176. [Google Scholar] [CrossRef] [PubMed]
- Cesar, P.H.S.; Braga, M.A.; Trento, M.V.C.; Menaldo, D.L.; Marcussi, S. Snake Venom Disintegrins: An Overview of their Interaction with Integrins. Curr. Drug Targets 2019, 20, 465–477. [Google Scholar] [CrossRef] [PubMed]
- Sanchez, E.E.; Rodriguez-Acosta, A.; Palomar, R.; Lucena, S.E.; Bashir, S.; Soto, J.G.; Perez, J.C. Colombistatin: A disintegrin isolated from the venom of the South American snake (Bothrops colombiensis) that effectively inhibits platelet aggregation and SK-Mel-28 cell adhesion. Arch. Toxicol. 2009, 83, 271–279. [Google Scholar] [CrossRef] [PubMed]
- Kumar, C.C.; Malkowski, M.; Yin, Z.; Tanghetti, E.; Yaremko, B.; Nechuta, T.; Varner, J.; Liu, M.; Smith, E.M.; Neustadt, B.; et al. Inhibition of angiogenesis and tumor growth by SCH221153, a dual αvβ3 and αvβ5 integrin receptor antagonist. Cancer Res. 2001, 61, 2232–2238. [Google Scholar] [PubMed]
- Al-Ostoot, F.H.; Salah, S.; Khamees, H.A.; Khanum, S.A. Tumor angiogenesis: Current challenges and therapeutic opportunities. Cancer Treat. Res. Commun. 2021, 28, 100422. [Google Scholar] [CrossRef] [PubMed]
- Weis, S.M.; Cheresh, D.A. Tumor angiogenesis: Molecular pathways and therapeutic targets. Nat. Med. 2011, 17, 1359–1370. [Google Scholar] [CrossRef] [PubMed]
- Akhtar, B.; Muhammad, F.; Sharif, A.; Anwar, M.I. Mechanistic insights of snake venom disintegrins in cancer treatment. Eur. J. Pharmacol. 2021, 899, 174022. [Google Scholar] [CrossRef] [PubMed]
- Kalita, B.; Saviola, A.J.; Mukherjee, A.K. From venom to drugs: A review and critical analysis of Indian snake venom toxins envisaged as anticancer drug prototypes. Drug Discov. Today 2021, 26, 993–1005. [Google Scholar] [CrossRef]
- Louis, D.N.; Ohgaki, H.; Wiestler, O.D.; Cavenee, W.K.; Burger, P.C.; Jouvet, A.; Scheithauer, B.W.; Kleihues, P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114, 97–109. [Google Scholar] [CrossRef]
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef]
- Dehelean, C.A.; Marcovici, I.; Soica, C.; Mioc, M.; Coricovac, D.; Iurciuc, S.; Cretu, O.M.; Pinzaru, I. Plant-Derived Anticancer Compounds as New Perspectives in Drug Discovery and Alternative Therapy. Molecules 2021, 26, 1109. [Google Scholar] [CrossRef]
- Huang, M.; Lu, J.J.; Ding, J. Natural Products in Cancer Therapy: Past, Present and Future. Nat. Prod. Bioprospecting 2021, 11, 5–13. [Google Scholar] [CrossRef]
- Newman, D.J.; Cragg, G.M. Natural Products as Sources of New Drugs over the Nearly Four Decades from 01/1981 to 09/2019. J. Nat. Prod. 2020, 83, 770–803. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.Z.; Zhu, Y.P.; Rahat, M.A.; Kzhyshkowska, J. Editorial: Angiogenesis and tumor metastasis. Front. Oncol. 2022, 12, 1129736. [Google Scholar] [CrossRef]
- Bielenberg, D.R.; Zetter, B.R. The Contribution of Angiogenesis to the Process of Metastasis. Cancer J. 2015, 21, 267–273. [Google Scholar] [CrossRef] [PubMed]
- Cross, M.J.; Claesson-Welsh, L. FGF and VEGF function in angiogenesis: Signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci. 2001, 22, 201–207. [Google Scholar] [CrossRef] [PubMed]
- Laddha, A.P.; Kulkarni, Y.A. VEGF and FGF-2: Promising targets for the treatment of respiratory disorders. Respir. Med. 2019, 156, 33–46. [Google Scholar] [CrossRef]
- Zhao, Y.; Adjei, A.A. Targeting Angiogenesis in Cancer Therapy: Moving Beyond Vascular Endothelial Growth Factor. Oncologist 2015, 20, 660–673. [Google Scholar] [CrossRef]
- Ansari, M.J.; Bokov, D.; Markov, A.; Jalil, A.T.; Shalaby, M.N.; Suksatan, W.; Chupradit, S.; Al-Ghamdi, H.S.; Shomali, N.; Zamani, A.; et al. Cancer combination therapies by angiogenesis inhibitors; a comprehensive review. Cell Commun. Signal. 2022, 20, 49. [Google Scholar] [CrossRef]
- Kolvekar, N.; Bhattacharya, N.; Sarkar, A.; Chakrabarty, D. How snake venom disintegrins affect platelet aggregation and cancer proliferation. Toxicon 2023, 221, 106982. [Google Scholar] [CrossRef]
- Leasher, J.L.; Bourne, R.R.; Flaxman, S.R.; Jonas, J.B.; Keeffe, J.; Naidoo, K.; Pesudovs, K.; Price, H.; White, R.A.; Wong, T.Y.; et al. Global Estimates on the Number of People Blind or Visually Impaired by Diabetic Retinopathy: A Meta-analysis From 1990 to 2010. Diabetes Care 2016, 39, 1643–1649. [Google Scholar] [CrossRef] [PubMed]
- Lee, R.; Wong, T.Y.; Sabanayagam, C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis. 2015, 2, 17. [Google Scholar] [CrossRef]
- Toh, H.; Smolentsev, A.; Bozadjian, R.V.; Keeley, P.W.; Lockwood, M.D.; Sadjadi, R.; Clegg, D.O.; Blodi, B.A.; Coffey, P.J.; Reese, B.E.; et al. Vascular changes in diabetic retinopathy-a longitudinal study in the Nile rat. Lab. Investig. 2019, 99, 1547–1560. [Google Scholar] [CrossRef]
- Stitt, A.W.; Curtis, T.M.; Chen, M.; Medina, R.J.; McKay, G.J.; Jenkins, A.; Gardiner, T.A.; Lyons, T.J.; Hammes, H.P.; Simo, R.; et al. The progress in understanding and treatment of diabetic retinopathy. Prog. Retin. Eye Res. 2016, 51, 156–186. [Google Scholar] [CrossRef] [PubMed]
- Gupta, N.; Mansoor, S.; Sharma, A.; Sapkal, A.; Sheth, J.; Falatoonzadeh, P.; Kuppermann, B.; Kenney, M. Diabetic retinopathy and VEGF. Open Ophthalmol. J. 2013, 7, 4–10. [Google Scholar] [CrossRef]
- Simo, R.; Sundstrom, J.M.; Antonetti, D.A. Ocular Anti-VEGF therapy for diabetic retinopathy: The role of VEGF in the pathogenesis of diabetic retinopathy. Diabetes Care 2014, 37, 893–899. [Google Scholar] [CrossRef] [PubMed]
- Moore, S.W.; Bhat, V.K.; Flatt, P.R.; Gault, V.A.; McClean, S. Isolation and characterisation of insulin-releasing compounds from Crotalus adamanteus, Crotalus vegrandis and Bitis nasicornis venom. Toxicon 2015, 101, 48–54. [Google Scholar] [CrossRef]
- Ramos, O.H.; Terruggi, C.H.; Ribeiro, J.U.; Cominetti, M.R.; Figueiredo, C.C.; Berard, M.; Crepin, M.; Morandi, V.; Selistre-de-Araujo, H.S. Modulation of in vitro and in vivo angiogenesis by alternagin-C, a disintegrin-like protein from Bothrops alternatus snake venom and by a peptide derived from its sequence. Arch. Biochem. Biophys. 2007, 461, 1–6. [Google Scholar] [CrossRef]
- Selistre-de-Araujo, H.S.; Pontes, C.L.; Montenegro, C.F.; Martin, A.C. Snake venom disintegrins and cell migration. Toxins 2010, 2, 2606–2621. [Google Scholar] [CrossRef]
- Gurtner, G.C.; Werner, S.; Barrandon, Y.; Longaker, M.T. Wound repair and regeneration. Nature 2008, 453, 314–321. [Google Scholar] [CrossRef]
- Zhao, R.; Liang, H.; Clarke, E.; Jackson, C.; Xue, M. Inflammation in Chronic Wounds. Int. J. Mol. Sci. 2016, 17, 2085. [Google Scholar] [CrossRef] [PubMed]
- Schnittert, J.; Bansal, R.; Storm, G.; Prakash, J. Integrins in wound healing, fibrosis and tumor stroma: High potential targets for therapeutics and drug delivery. Adv. Drug Deliv. Rev. 2018, 129, 37–53. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, B.A.; Deconte, S.R.; de Moura, F.B.R.; Tomiosso, T.C.; Clissa, P.B.; Andrade, S.P.; Araujo, F.A. Inflammation, angiogenesis and fibrogenesis are differentially modulated by distinct domains of the snake venom metalloproteinase jararhagin. Int. J. Biol. Macromol. 2018, 119, 1179–1187. [Google Scholar] [CrossRef] [PubMed]
- Sant’Ana, E.M.; Gouvea, C.M.; Durigan, J.L.; Cominetti, M.R.; Pimentel, E.R.; Selistre-de-Araujo, H.S. Rat skin wound healing induced by alternagin-C, a disintegrin-like, Cys-rich protein from Bothrops alternatus venom. Int. Wound J. 2011, 8, 245–252. [Google Scholar] [CrossRef] [PubMed]
- Rabelo, L.F.G.; Ferreira, B.A.; Deconte, S.R.; Tomiosso, T.C.; Dos Santos, P.K.; Andrade, S.P.; Selistre de Araujo, H.S.; Araujo, F.A. Alternagin-C, a disintegrin-like protein from Bothrops alternatus venom, attenuates inflammation and angiogenesis and stimulates collagen deposition of sponge-induced fibrovascular tissue in mice. Int. J. Biol. Macromol. 2019, 140, 653–660. [Google Scholar] [CrossRef]
- Turner, C.J.; Badu-Nkansah, K.; Crowley, D.; van der Flier, A.; Hynes, R.O. α5 and αv integrins cooperate to regulate vascular smooth muscle and neural crest functions in vivo. Development 2015, 142, 797–808. [Google Scholar] [CrossRef] [PubMed]
- Topol, E.J.; Byzova, T.V.; Plow, E.F. Platelet GPIIb-IIIa blockers. Lancet 1999, 353, 227–231. [Google Scholar] [CrossRef] [PubMed]
- Hartman, G.D.; Egbertson, M.S.; Halczenko, W.; Laswell, W.L.; Duggan, M.E.; Smith, R.L.; Naylor, A.M.; Manno, P.D.; Lynch, R.J.; Zhang, G.; et al. Non-peptide fibrinogen receptor antagonists. 1. Discovery and design of exosite inhibitors. J. Med. Chem. 1992, 35, 4640–4642. [Google Scholar] [CrossRef]
- Almeida, G.O.; de Oliveira, I.S.; Arantes, E.C.; Sampaio, S.V. Snake venom disintegrins update: Insights about new findings. J. Venom. Anim. Toxins Incl. Trop. Dis. 2023, 29, e20230039. [Google Scholar] [CrossRef]
- Lang, S.H.; Manning, N.; Armstrong, N.; Misso, K.; Allen, A.; Di Nisio, M.; Kleijnen, J. Treatment with tirofiban for acute coronary syndrome (ACS): A systematic review and network analysis. Curr. Med. Res. Opin. 2012, 28, 351–370. [Google Scholar] [CrossRef]
- Bordon, K.C.F.; Cologna, C.T.; Fornari-Baldo, E.C.; Pinheiro-Junior, E.L.; Cerni, F.A.; Amorim, F.G.; Anjolette, F.A.P.; Cordeiro, F.A.; Wiezel, G.A.; Cardoso, I.A.; et al. From Animal Poisons and Venoms to Medicines: Achievements, Challenges and Perspectives in Drug Discovery. Front. Pharmacol. 2020, 11, 1132. [Google Scholar] [CrossRef]
- Scarborough, R.M.; Rose, J.W.; Hsu, M.A.; Phillips, D.R.; Fried, V.A.; Campbell, A.M.; Nannizzi, L.; Charo, I.F. Barbourin. A GPIIb-IIIa-specific integrin antagonist from the venom of Sistrurus m. barbouri. J. Biol. Chem. 1991, 266, 9359–9362. [Google Scholar] [CrossRef]
- Roth, G.A.; Huffman, M.D.; Moran, A.E.; Feigin, V.; Mensah, G.A.; Naghavi, M.; Murray, C.J. Global and regional patterns in cardiovascular mortality from 1990 to 2013. Circulation 2015, 132, 1667–1678. [Google Scholar] [CrossRef]
- Podrez, E.A.; Byzova, T.V.; Febbraio, M.; Salomon, R.G.; Ma, Y.; Valiyaveettil, M.; Poliakov, E.; Sun, M.; Finton, P.J.; Curtis, B.R.; et al. Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype. Nat. Med. 2007, 13, 1086–1095. [Google Scholar] [CrossRef] [PubMed]
- Venturini, W.; Olate-Briones, A.; Valenzuela, C.; Mendez, D.; Fuentes, E.; Cayo, A.; Mancilla, D.; Segovia, R.; Brown, N.E.; Moore-Carrasco, R. Platelet Activation Is Triggered by Factors Secreted by Senescent Endothelial HMEC-1 Cells In Vitro. Int. J. Mol. Sci. 2020, 21, 3287. [Google Scholar] [CrossRef] [PubMed]
- Huilcaman, R.; Venturini, W.; Fuenzalida, L.; Cayo, A.; Segovia, R.; Valenzuela, C.; Brown, N.; Moore-Carrasco, R. Platelets, a Key Cell in Inflammation and Atherosclerosis Progression. Cells 2022, 11, 1014. [Google Scholar] [CrossRef] [PubMed]
- Bledzka, K.; Smyth, S.S.; Plow, E.F. Integrin αIIbβ3: From discovery to efficacious therapeutic target. Circ. Res. 2013, 112, 1189–1200. [Google Scholar] [CrossRef] [PubMed]
- Rivas-Mercado, E.A.; Garza-Ocañas, L. Disintegrins obtained from snake venom and their pharmacological potential. Med. Univ. 2017, 19, 32–37. [Google Scholar] [CrossRef]
- Canas, C.A.; Castano-Valencia, S.; Castro-Herrera, F.; Canas, F.; Tobon, G.J. Biomedical applications of snake venom: From basic science to autoimmunity and rheumatology. J. Transl. Autoimmun. 2021, 4, 100076. [Google Scholar] [CrossRef] [PubMed]
- Cook, J.J.; Huang, T.F.; Rucinski, B.; Strzyzewski, M.; Tuma, R.F.; Williams, J.A.; Niewiarowski, S. Inhibition of platelet hemostatic plug formation by trigramin, a novel RGD-peptide. Am. J. Physiol. 1989, 256, H1038–H1043. [Google Scholar] [CrossRef] [PubMed]
- Monteiro, D.A.; Kalinin, A.L.; Selistre-de-Araujo, H.S.; Vasconcelos, E.S.; Rantin, F.T. Alternagin-C (ALT-C), a disintegrin-like protein from Rhinocerophis alternatus snake venom promotes positive inotropism and chronotropism in fish heart. Toxicon 2016, 110, 1–11. [Google Scholar] [CrossRef] [PubMed]
Name (Source) | Recognizing Motif | Physiological Target | Angiogenic Factors | References |
---|---|---|---|---|
Jararhagin-C | ECD-disintegrin-like/cysteine-rich domains | Interferes with α2β1 integrin functions | Pro-angiogenic | [8] |
Alternagina-C | Exhibits both pro- and anti-angiogenic effects | [29,50,51] | ||
Leberagin-C | Disintegrin-like | Interferes with αvβ3, αvβ6, and α5β1 integrins | Anti-angiogenesis | [52] |
Echistatin | RGD-dependent disintegrins | Binds to integrin αIIbβ3, GPIIb/IIIa and interacts with αvβ3 integrin | Anti-angiogenesis | [14,32,53] |
Rhodostomin | [49] | |||
Contortrostatin | Interacts with the integrins αvβ3 and α5β1 | [37] | ||
Vicrostatin | antagonize the function of the αIIbβ3, αvβ3, αvβ5 and α5β1 integrins | [23] | ||
DisBa-01 | Binds to integrin αvβ3 | [54] | ||
Aggretin | Binds to integrin α2β1 | Pro-angiogenic | [55] | |
Trigramin | Binds to αIIbβ3, α8β1, αvβ3, αvβ5 and/or α5β1 integrins | [56] | ||
Obtustatin | KTS-disintegrin | Selectively inhibit α1β1-integrin | Anti-angiogenesis | [46] |
Viperistatin | Inhibitory activity against collagen receptors, α1β1 and α2β1-integrins | [47] | ||
Lebestatin | Inhibis binding of α1β1 integrin to type IV and type I collagen | [42] | ||
Jerdostatin | RTS-disintegrin | Antagonizes the function of the α1β1 integrin | Anti-angiogenesis | [48] |
Agkistin-s | InteractS with GPIB | Anti-angiogenesis | [57] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Clissa, P.B.; Della-Casa, M.S.; Zychar, B.C.; Sanabani, S.S. The Role of Snake Venom Disintegrins in Angiogenesis. Toxins 2024, 16, 127. https://doi.org/10.3390/toxins16030127
Clissa PB, Della-Casa MS, Zychar BC, Sanabani SS. The Role of Snake Venom Disintegrins in Angiogenesis. Toxins. 2024; 16(3):127. https://doi.org/10.3390/toxins16030127
Chicago/Turabian StyleClissa, Patricia Bianca, Maisa Splendore Della-Casa, Bianca Cestari Zychar, and Sabri Saeed Sanabani. 2024. "The Role of Snake Venom Disintegrins in Angiogenesis" Toxins 16, no. 3: 127. https://doi.org/10.3390/toxins16030127
APA StyleClissa, P. B., Della-Casa, M. S., Zychar, B. C., & Sanabani, S. S. (2024). The Role of Snake Venom Disintegrins in Angiogenesis. Toxins, 16(3), 127. https://doi.org/10.3390/toxins16030127