Angiogenesis, Inflammation & Therapeutics | Online ISSN  2207-872X
REVIEWS   (Open Access)

Microbial Avengers: How Microorganisms Drive Angiogenesis for Good and Bad?

Md. Fakruddin1*, Zarifah Chowdhury1, Sayed Ul Alam Shibly2, SM Bakhtiar Ul Islam1, Jinath Sultana Jime1, Nayeema Bulbul1, Mohammad Badrul Anam3, Khanjada Shahnewaj Bin Mannan4, Md. Asaduzzaman Shishir5

+ Author Affiliations

Journal of Angiotherapy 8(5) 1-12 https://doi.org/10.25163/angiotherapy.859650

Submitted: 04 March 2024  Revised: 01 May 2024  Published: 05 May 2024 

Abstract

Angiogenesis is the formation of new blood vessels from pre-existing ones, and it plays a pivotal role in both the initiation and spread of cancer. Microorganisms have been recognized as influential regulators of angiogenesis, with certain strains fostering (angiogenic) while others impeding (antiangiogenic) this biological process. According to recent studies, microbes can control angiogenesis via various pathways, making them intriguing options for therapies meant to prevent cancer growth. This review provides a comprehensive overview of current understanding regarding how microbes modulate angiogenesis in cancer. It emphasizes the involvement of different bacterial and fungal species and elucidates the mechanisms through which they exert their effects. This review addresses how numerous microbes produce diverse bioactive substances that suppress the BCL-2 gene, leading to the disruption of mitochondrial outer membranes. Consequently, the release of cytochrome c from mitochondria serves to inhibit angiogenesis through the formation of the apoptosome, a complex involving cytochrome c, Apaf-1, and procaspase-9, which catalyzes the activation of caspases. Ultimately, this cascade of events culminates in programmed cell death, thereby impeding the process of angiogenesis. Some bacteria produce proteins like basic fibroblast growth factor (bFGF) and vascular endothelial growth factor (VEGF), promoting angiogenesis whereas certain bacteria induce angiogenesis by decreasing microRNA-203a levels, leading to increased production of proangiogenic factors which facilitates angiogenesis. Proangiogenic bacteria show promise in tissue regeneration and addressing vision impairment. These findings indicate potential for novel strategies to improve healing and vision in patients with diverse medical conditions. Nevertheless, additional investigation is required to refine the effectiveness and safety profiles of these bacterial-derived therapies for eventual clinical implementation. This review highlights the yet-to-be-explored capacity of microorganisms in cancer treatment through the suppression of angiogenesis, paving the way for innovative therapeutic strategies that could yield highly potent anti-cancer medications.

Keywords: Microbiome, Angiogenesis, Promote, Inhibit, Cancer.

References

Adiyoga, R., Arief, I. I., Budiman, C., & Abidin, Z. (2022). In vitro anticancer potentials of Lactobacillus plantarum IIA-1A5 and Lactobacillus acidophilus IIA-2B4 extracts against WiDr human colon cancer cell line. Food Science and Technology, 42, e87221. https://doi.org/10.1590/fst.87221

 

Al-deeb, I., Joseph, J., Majid, A. M. S. A., & Samad N. A. (2021). Phytochemicals with Direct and/or Indirect Anti-angiogenic Properties Against Various Cancer Types Focusing on Their Mechanism of Action. Journal of Angiotherapy, 5(1), 226-233. https://doi.org/10.25163/angiotherapy.51212406111121

 

Al-Ostoot, F. H., Salah, S., Khamees, H. A., & Khanum, S. A.  (2021). Tumor angiogenesis: Current challenges and therapeutic opportunities. Cancer Treatment and Research Communications, 28, 100422. Doi: https://doi.org/10.1016/j.ctarc.2021.100422

 

Al-Rawi, S. S., Ibrahim, A. H., Hamde, M. A., Babu, D., Nazari, M., Ab Kadir, M. O., Majid, A. S. A., & Shah, A. M. (2023). Antiangiogenic and Anticancer Potential of Supercritical Fluid Extracts from Nutmeg Seeds; In vitro, Ex vivo and In silico studies. Journal of Angiotherapy, 7(1), 1-13. https://doi.org/10.25163/angiotherapy.719371

 

Al-Suede, F. S. R., Ahamed, M. B. K., Majid, A. S. A.,   Saghir, S. A. M.,  Oon, C. E., & Majid, A. M. S. A. (2021). Immunomodulatory and Antiangiogenic Mechanisms of Polymolecular Botanical Drug Extract C5OSEW5050ESA OS Derived from Orthosiphon stamineus. Journal of Angiotherapy, 5(1), 194-206. https://doi.org/10.25163/angiotherapy.51211411913130321

 

Alipour, M. (2020). Molecular mechanism of Helicobacter pylori- Induced gastric Cancer. Journal of Gastrointestinal Cancer, 52(1), 23–30. https://doi.org/10.1007/s12029-020-00518-5

 

Almanaa, T. N., Yassin, M. A., El-Mekkawy, R. M., Ahmed, N. S., & Rabie, G. H. (2020). Anticancer and Antioxidant Activity by Secondary Metabolites of Aspergillus fumigatus Advances in Animal and Veterinary Sciences, 9(2), 265-273. https://doi.org/10.17582/journal.aavs/2021/9.2.265.273

 

Amin, T., Karim, A. B., Oyshe, I. I., Hossain, A., Karim, T., Jime, J. S., ….& Fakruddin, M. (2023). Unlocking Nature’s Treasure Trove: Exploring Microorganisms for Novel Bioactives, Journal of Angiotherapy, 7(1), 1-8. Doi: https://doi.org/10.25163/angiotherapy.719345

 

Ansari, M. J., Bokov, D., Markov, A., Jalil, A. T., Shalaby, M. N., Suksatan, W., …. & Dadashpour, M. (2022). Cancer combination therapies by angiogenesis inhibitors; a comprehensive review. Cell Communication and Signaling, 20(1), 49. https://doi.org/10.1186/s12964-022-00838-y

 

Anwar, M. M., Albanese, C., Hamdy, N. M., & Sultan, A. S. (2022). Rise of the natural red pigment ‘prodigiosin’ as an immunomodulator in cancer. Cancer Cell International, 22(1), 419. https://doi.org/10.1186/s12935-022-02815-4

 

Bajuri, U. K. M., Ramasamy, K., & Lim, S. M. (2022). Cytotoxic and Anti-angiogenic Effects of Postbiotics Derived from Pediococcus spp. against CT26 Mouse Colon Carcinoma Cells. Journal of Angiotherapy, 6(3), 723. https://doi.org/10.25163/angiotherapy.6341C

 

Belkaid, Y., & Hand, T. W. (2014). Role of the microbiota in immunity and inflammation. Cell, 157(1), 121–141. https://doi.org/10.1016/j.cell.2014.03.011

 

Bergers, G., & Benjamin, L. E. (2003). Tumorigenesis and the angiogenic switch. Nature Reviews Cancer, 3(6), 401–410. https://doi.org/10.1038/nrc1093

 

Bhatt, A. P., Redinbo, M. R., & Bultman, S. J. (2017). The role of the microbiome in cancer development and therapy. CA Cancer Journal for Clinicians, 67(4), 326-344. doi: 10.3322/caac.21398  

 

Carmeliet, P., & Jain, R. K. (2000). Angiogenesis in cancer and other diseases. Nature, 407(6801), 249–257. https://doi.org/10.1038/35025220

 

Carmeliet, P., & Jain, R. K. (2011a). Molecular mechanisms and clinical applications of angiogenesis. Nature, 473(7347), 298–307. https://doi.org/10.1038/nature10144

 

Carmeliet, P., & Jain, R. K. (2011b). Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nature Reviews Drug Discovery, 10(6), 417–427. https://doi.org/10.1038/nrd3455

 

Cerimele, F., Brown, L. F., Bravo, F., Ihler, G. M., Kouadio, P., & Arbiser, J. L. (2003). Infectious Angiogenesis: Bartonella bacilliformis Infection Results in Endothelial Production of Angiopoetin-2 and Epidermal Production of Vascular Endothelial Growth Factor. American Journal of Pathology, 163(4), 1321-1327. https://doi.org/10.1016/S0002-9440(10)63491-8

 

Chang, E. L., Ting, C. Y., Hsu, P.H., Lin, Y. C., Liao, E. C., Huang, C. Y., …. & Yeh, C. K. (2017). Angiogenesis-targeting microbubbles combined with ultrasound-mediated gene therapy in brain tumors. The Journal of Controlled Release, 255, 164-175. doi: 10.1016/j.jconrel.2017.04.010

 

Chu, Y. C., Chang, C., Liao, H. R., Fu, S. L., & Chen, J. J. (2021). Anti-Cancer and Anti-Inflammatory Activities of Three New Chromone Derivatives from the Marine-Derived Penicillium citrinum. Marine Drugs, 19(8), 408. https://doi.org/10.3390/md19080408
 

Dabrowska, K., & Witkiewicz, W. (2016). Correlations of Host Genetics and Gut Microbiome Composition. Frontiers in Microbiology, 7, 1357. DOI:10.3389/fmicb.2016.01357   

de Menezes, A-A. P. M., Aguiar, R. P. S., Santos, J. V. O., Sarkar, C., Islam, M. T., Braga, A. L., …. & Sousa, J. M. C. (2023). Citrinin as a potential anti-cancer therapy: A comprehensive review. Chemico-Biological Interactions, 381, 110561. Doi: https://doi.org/10.1016/j.cbi.2023.110561

 

DeBritto, S., Gajbar, T. D., Satapute, P., Sundaram, L., Lakshmikantha, R. Y., Jogaiah, S., & Ito, S-I. (2020). Isolation and characterization of nutrient dependent pyocyanin from Pseudomonas aeruginosa and its dye and agrochemical properties. Scientific Reports, 10(1), 1542. https://doi.org/10.1038/s41598-020-58335-6

 

Dehghani, N., Tafvizi, F., & Jafari, P. (2020). Cell cycle arrest and anti-cancer potential of probiotic Lactobacillus rhamnosus against HT-29 cancer cells. Bioimpacts, 11(4), 245–252. https://doi.org/10.34172/bi.2021.32

 

Faghfoori, Z., Faghfoori, M. H., Saber, A., Izadi, A., & Khosroushahi, A. Y. (2021). Anticancer effects of bifidobacteria on colon cancer cell lines. Cancer Cell International, 21(1), 258. https://doi.org/10.1186/s12935-021-01971-3

 

Fakruddin, M., Shishir, M. A., Oyshe, I. I., Amin, S. M. T., Hossain, A., Sarna, I. I., Jerin, N., & Mitra, D. K. (2023). Microbial Architects of Malignancy: Exploring the Gut Microbiome’s Influence in Cancer Initiation and Progression. Cancer Plus, 5(1), 1. https://doi.org/10.18063/cp.397

 

Fakruddin, M., Shishir, M. A., Mouree, K. R., & Khan, S. S. (2022). Environmental and physiological angiogenesis in causing CVD with oxidative pattern. Journal of Angiotherapy, 6(2), 663-667. https://doi.org/10.25163/angiotherapy.622129

 

Fakruddin, M., Shishir, M. A., Yousuf, Z., & Khan, S. S. (2022). Next Generation Probiotics- The Future of Biotherapeutics. Microbial Bioactives, 5(1), 156-163. DOI: https://doi.org/10.25163/microbbioacts.514309

 

Ferrara, N. (2002). VEGF and the quest for tumour angiogenesis factors. Nature Reviews Cancer, 2(10), 795–803. https://doi.org/10.1038/nrc909
 

Ferrara, N., & Adamis, A. P. (2016). Ten years of anti-vascular endothelial growth factor therapy. Nature Reviews Drug Discovery, 15(6), 385–403. https://doi.org/10.1038/nrd.2015.17
 

Folkman, J. (1995). Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Medicine, 1(1), 27–30. https://doi.org/10.1038/nm0195-27
 

Francescone, R., Hou, V., & Grivennikov, S. I. (2014). Microbiome, inflammation, and cancer. Cancer Journal, 20(3), 181-189. doi: 10.1097/PPO.0000000000000048
 

Franks, I. (2013). Gut microbes might promote intestinal angiogenesis. Nature Reviews Gastroenterology & Hepatology, 10, 3. https://doi.org/10.1038/nrgastro.2012.227

 

Gopalakrishnan, V., Weiner, B., Ford, C. B., Sellman, B. R., Hammond, S. A., Freeman, D. J., …. & Henn, M. R. (2020). Intervention strategies for microbial therapeutics in cancer immunotherapy. Immuno-Oncology Technology, 6, 9-17. Doi: https://doi.org/10.1016/j.iotech.2020.05.001
 

Gouda, S., Das, G., Sen, S. K., Shin, H., & Patra, J. K. (2016). Endophytes: a treasure house of bioactive compounds of medicinal importance. Frontiers in Microbiology, 7, 1538. https://doi.org/10.3389/fmicb.2016.01538
 

Guruceaga, X., Perez-Cuesta, U., Pellon, A., Cendon-Sanchez, S., Pelegri-Martinez, E., Gonzalez, O., …. & Rementeria, A. (2021). Aspergillus fumigatus Fumagillin Contributes to Host Cell Damage. Journal of Fungi, 7(11), 936. doi: 10.3390/jof7110936

 

Han, J. M., Jang, J. P., Jang, J. H., Ahn, J. S., & Jung, H. J. (2020). Antiangiogenic potentials of ahpatinins obtained from a Streptomyces species. Oncology Reports, 43(2), 625-634. doi: 10.3892/or.2019.7446

 

Hanahan, D., & Weinberg, R. A. (2011). Hallmarks of Cancer: The next generation. Cell, 144(5), 646–674. https://doi.org/10.1016/j.cell.2011.02.013
 

Hashemi-Khah, M., Soleimani, N. A., Forghanifard, M. M., Gholami, O., Taheri, S., & Amoueian, S. (2022). An In Vivo Study of Lactobacillus rhamnosus (PTCC 1637) as a New Therapeutic Candidate in Esophageal Cancer. BioMed Research International, 2022, 1–9. https://doi.org/10.1155/2022/7607470

 

Hassan, M., Elmezain, W. A., Baraka, D., Abo-Elmaaty, S. A., Elhassanein, A., Ibrahim, R. M., & Hamed, A. A. (2024). Anti-Cancer and Anti-Oxidant Bioactive Metabolites from Aspergillus fumigatus WA7S6 Isolated from Marine Sources: In Vitro and In Silico Studies. Microorganisms, 12(1), 127. https://doi.org/10.3390/microorganisms12010127

 

Ho, T. F., Peng, Y., Chuang, S., Lin, S. C., Feng, B., Lu, C., …. & Chang, C. (2009). Prodigiosin down-regulates survivin to facilitate paclitaxel sensitization in human breast carcinoma cell lines. Toxicology and Applied Pharmacology, 235(2), 253–260. https://doi.org/10.1016/j.taap.2008.12.009
 

Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268–1273. https://doi.org/10.1126/science.1223490

 

Jain, R. K. (2014). Anti-angiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell, 26(5), 605-622. doi:10.1016/j.ccell.2014.10.006  

 

Jain, R. K., Duda, D. G., Willett, C. G., Sahani, D. V., Zhu, A. X., Loeffler, J. S., Batchelor, T. T., & Sorensen, A. G. (2009). Biomarkers of response and resistance to antiangiogenic therapy. Nature Reviews Clinical Oncology, 6(6), 327–338. https://doi.org/10.1038/nrclinonc.2009.63
 

Jang, J., Han, J. M., Jung, H. J., Osada, H., Jang, J., & Ahn, J. S. (2018). Anti-Angiogenesis Effects Induced by Octaminomycins A and B against HUVECs. Journal of Microbiology and Biotechnology, 28(8), 1332-1338. https://doi.org/10.4014/jmb.1806.06046

 

Jang, J., Jang, M., Nogawa, T., Takahashi, S., Osada, H., Ahn, J. S., Ko, S., & Jang, J. (2022).  RK-270D and E, Oxindole Derivatives from Streptomyces sp. with Anti-Angiogenic Activity.  Journal of Microbiology and Biotechnology, 32, 302-306.  https://doi.org/10.4014/jmb.2110.10039

 

Kerbel, R.S. (2008). Tumor angiogenesis. New England Journal of Medicine, 358(19), 2039-2049. doi: 10.1056/NEJMra0706596
 

Kerbel, R. S. (2011). Improving conventional or targeted anticancer therapy with complementary, not alternative, antiangiogenic treatment strategies. Journal of Clinical Oncology, 29(10), 1239-1242. doi: 10.1200/JCO.2010.32.9504

 

Konishi, H., Fujiya, M., Tanaka, H., Ueno, N., Moriichi, K., Sasajima, J., …. & Kohgo, Y. (2016). Probiotic-derived ferrichrome inhibits colon cancer progression via JNK-mediated apoptosis. Nature Communications, 7(1), 12365. https://doi.org/10.1038/ncomms12365
 

Lei, Z. N., Teng, Q. X., Tian, Q., Chen, W., Xie, Y., Wu, K., …. & He, Y. (2022). Signaling pathways and therapeutic interventions in gastric cancer. Signal Transduction and Targeted Therapy, 7, 358. https://doi.org/10.1038/s41392-022-01190-w

 

Liberto, M. C., Matera, G., Lamberti, A. G., Barreca, G. S., Quirino, A., & Focà, A. (2003). In vitro Bartonella quintana infection modulates the programmed cell death and inflammatory reaction of endothelial cells. Diagnostic Microbiology and Infectious Disease, 45(2), 107–115. https://doi.org/10.1016/s0732-8893(02)00461-3

 

Liu, Z-L., Chen, H-H., Zheng, L-L., Sun, L-P., Shi, L. (2023).  Angiogenic signaling pathways and anti-angiogenic therapy for cancer. Signal Transduction and Targeted Therapy, 8, 198. https://doi.org/10.1038/s41392-023-01460-1

 

Lok, B. (2017). Angiogenesis and its potential role in the growth and proliferation of pathogens. Journal of Angiotherapy, 1(1), E001-E011. https://doi.org/10.25163/angiotherapy.11000121421300417

--

Malespín-Bendaña, W., Ferreira, R. M., Pinto, M., Figueiredo, C., Alpízar-Alpízar, W., Une, C., Figueroa-Protti, L., & RamíRez, V. (2023). Helicobacter pylori infection induces abnormal expression of pro-angiogenic gene ANGPT2 and miR-203a in AGS gastric cell line. Brazilian Journal of Microbiology, 54(2), 791–801. https://doi.org/10.1007/s42770-023-00940-4
 

Marmé, D. (2018). Tumor Angiogenesis: A Key Target for Cancer Therapy. Oncology Research and Treatment,  41 (4), 164. https://doi.org/10.1159/000488340

 

Mudaliar, S. B., & Prasad, A. S. B. (2024). A biomedical perspective of pyocyanin from Pseudomonas aeruginosa: its applications and challenges. World Journal of Microbiology & Biotechnology, 40(3), 90. https://doi.org/10.1007/s11274-024-03889-0

 

Mueller, A., Brockmueller, A., Fahimi, N., Ghotbi, T., Hashemi, S., Sadri, S., …. & Shakibaei, M. (2022). Bacteria-Mediated Modulatory Strategies for Colorectal Cancer treatment. Biomedicines, 10(4), 832. https://doi.org/10.3390/biomedicines10040832

 

Nafsi, N. N., Rahman, M. A., Shishir, M. A., Arefin, M. S., Jime, J. S., Bulbul, N., Safa, A., & Fakruddin, M. (2024). Unleashing the Potential of Gut Microbiota: Cholesterol Reduction Through Microbial Bile Acid Metabolism. Current Biotechnology, 13(1), 6-14. Doi: 10.2174/0122115501282536240301055402

 

Naidu, J. R., Sreenivasan, S., Ruhi, S., Chen, H. W. J., Naidu, S. R., Khan, D., Aung, T. T., Thwin, M. M., Al-Goshae, H. A., & Rammohan, S. (2023). Review on Angiogenesis Modulation by Natural Compounds as Therapeutic Potential and Mechanisms. Journal of Angiotherapy, 8(2), 1-6. https://doi.org/10.25163/angiotherapy.829507

 

Osherov, N., & Ben-Ami, R. (2016). Modulation of Host Angiogenesis as a Microbial Survival Strategy and Therapeutic Target. PLoS Pathogens, 12(4), e1005479. doi: 10.1371/journal.ppat.1005479

Potente, M., Gerhardt, H., & Carmeliet, P. (2011). Basic and therapeutic aspects of angiogenesis. Cell, 146(6), 873–887. https://doi.org/10.1016/j.cell.2011.08.039
 

Procaccianti, G., Roggiani, S., Conti, G., Brigidi, P., Turroni, S., & D'Amico, F. (2023). Bifidobacterium in anticancer immunochemotherapy: friend or foe? Microbiome Research Reports, 2(3), 24. doi: 10.20517/mrr.2023.23

 

Rajoka, M. S. R., Zhao, H., Mehwish, H. M., Li, N., Lü, Y., Lian, Z., …. & Shi, J. (2019). Anti-tumor potential of cell free culture supernatant of Lactobacillus rhamnosus strains isolated from human breast milk. Food Research International, 123, 286–297. https://doi.org/10.1016/j.foodres.2019.05.002

 

Rooks, M., & Garrett, W. S. (2016). Gut microbiota, metabolites and host immunity. Nature Reviews Immunology, 16(6), 341–352. https://doi.org/10.1038/nri.2016.42

 

Sajib, S., Zahra, F. T., Lionakis, M. S., German, N., & Mikelis, C. M. (2017). Mechanisms of angiogenesis in microbe-regulated inflammatory and neoplastic conditions. Angiogenesis, 21(1), 1–14. https://doi.org/10.1007/s10456-017-9583-4

 

Sankarapandian, V., Maran, B. A. V., Rajendran, R. L., Jogalekar, M. P., Sridharan, G., Krishnamoorthy, R., Gangadaran, P., & Ahn, B. (2022). An update on the effectiveness of probiotics in the prevention and treatment of cancer. Life, 12(1), 59. https://doi.org/10.3390/life12010059

 

Sater, A. H. A., Bouferraa, Y., Amhaz, G., Haibe, Y., Lakkiss, A. E., & Shamseddine, A. (2022). From Tumor Cells to Endothelium and Gut Microbiome: A Complex Interaction Favoring the Metastasis Cascade. Frontiers in Oncology, 12, 804983. doi:10.3389/fonc.2022.804983

 

Sawant, S. S., Patil, S. M., Gupta, V., & Kunda, N. K. (2020). Microbes as Medicines: Harnessing the power of bacteria in advancing Cancer treatment. International Journal of Molecular Sciences, 21(20), 7575. https://doi.org/10.3390/ijms21207575

 

Schirbel, A., Kessler, S., Rieder, F., West, G., Rebert, N., Asosingh, K., McDonald, C., & Fiocchi, C. (2013). Pro-Angiogenic Activity of TLRs and NLRs: A Novel Link Between Gut Microbiota and Intestinal Angiogenesis. Gastroenterology, 144(3), 613-623.e9. Doi: https://doi.org/10.1053/j.gastro.2012.11.005

 

Schwabe, R. F., & Jobin, C. (2013). The microbiome and cancer. Nature Reviews Cancer. 13(11), 800-812. doi:10.1038/nrc3610

 

Sethi, Y., Vora, V., Anyagwa, O. E., Turabi, N., Abdelwahab, M., Kaiwan, O., …. & Padda, I. (2024). Streptomyces Paradigm in Anticancer therapy: A State-of-the Art review. Current Cancer Therapy Reviews, 20(4), 386-401.  Doi: 10.2174/0115733947254550230920170230 

 

Sevcikova, A., Mladosievicova, B., Mego, M., & Ciernikova, S. (2023). Exploring the role of the gut and intratumoral microbiomes in tumor progression and metastasis. International Journal of Molecular Sciences, 24(24), 17199.

 

Sherwood, L. M., Parris, E. E., & Folkman, J. (1971). Tumor angiogenesis: therapeutic implications. The New England Journal of Medicine, 285(21), 1182–1186. https://doi.org/10.1056/nejm197111182852108

 

Shishir, M. A., Sultana, S., Turna, J. T., Akter, T., Mim, S. J., Islam, R., & Fakruddin, M. (2023). Non-Ribosomally Synthesized Lipopeptides (NRLP): Novel Potential Therapeutics for Cancer Treatment. Cancer Plus, 5(2), 2569. https://doi.org/10.36922/cp.2569

 

Somani, R. R., & Bhanushali, U. V. (2013). Targeting angiogenesis for treatment of human cancer. Indian Journal of Pharmaceutical Sciences, 75(1), 3-10. doi: 10.4103/0250-474X.113529  

 

Tran, P. M., Tang, S., & Salgado-Pabón, W. (2022). Staphylococcus aureus β-Toxin Exerts Anti-angiogenic Effects by Inhibiting Re-endothelialization and Neovessel Formation. Frontiers in Microbiology, 13, 840236. https://doi.org/10.3389/fmicb.2022.840236

 

Tsukamoto, K., Kumadaki, K., Tatematsu, K., Suzuki, N., & Doi, Y. (2022). The of Bartonella bacilliformis BafA Promotes Endothelial Cell Angiogenesis via the VEGF Receptor Signaling Pathway. mSphere, 7(2), e0008122. doi: 10.1128/msphere.00081-22

 

Tsukamoto, K., Shinzawa, N., Kawai, A., Suzuki, M., Kidoya, H., Takakura, N., …. & Doi, Y. (2020). The Bartonella autotransporter BafA activates the host VEGF pathway to drive angiogenesis. Nature Communications, 11(1), 3571. https://doi.org/10.1038/s41467-020-17391-2
 

Uusi-Mäkelä, M., & Rämet, M. (2018). Hijacking host angiogenesis to drive mycobacterial growth. Cell Host & Microbe, 24(4), 465–466. https://doi.org/10.1016/j.chom.2018.09.016

 

Vadlapudi, V., Borah, N., Yellusani, K. R., Gade, S., Reddy, P. S. R., Rajamanikyam, M., …. & Amanchy, R. (2017). Aspergillus Secondary Metabolite Database, a resource to understand the Secondary metabolome of Aspergillus genus. Scientific Reports, 7(1), 7325. https://doi.org/10.1038/s41598-017-07436-w

 

Vieira, A. T., Teixeira, M. M., & Martins, F.S. (2013). The Role of Probiotics and Prebiotics in Inducing Gut Immunity. Frontiers in Immunology, 4, 445. doi: 10.3389/fimmu.2013.00445

 

Visconti, A., Roy, C. I. L., Rosa, F., Rossi, N., Martin, T., Mohney, R. P., …. & Falchi, M. (2019). Interplay between the human gut microbiome and host metabolism. Nature Communications, 10(1), 4505. https://doi.org/10.1038/s41467-019-12476-z
 

Wan, X., Song, M., Wang, A., Zhao, Y., Wei, Z., & Lu, Y. (2021). Microbiome Crosstalk in Immunotherapy and Anti-angiogenesis Therapy. Frontiers in Immunology, 12, 747914. doi: 10.3389/fimmu.2021.747914

 

Xue, C., Li, G., Gu, X., Su, Y., Zheng, Q., Yuan, X., Bao, Z., Lu, J., & Li, L. (2023). Health and Disease: Akkermansia muciniphila, the Shining Star of the Gut Flora. Research (Wash D C), 6, 0107. doi: 10.34133/research.0107

 

Yoda, K., Miyazawa, K., Hosoda, M., Hiramatsu, M., Yan, F., & He, F. (2013). Lactobacillus GG-fermented milk prevents DSS-induced colitis and regulates intestinal epithelial homeostasis through activation of epidermal growth factor receptor. European Journal of Nutrition, 53(1), 105–115. https://doi.org/10.1007/s00394-013-0506-x
 

Zhao, L-Y., Mei, J-X., Yu, G., Lei, L., Zhang, W-H, Liu, K., …. & Hu, J-K.  (2023). Role of the gut microbiota in anticancer therapy: from molecular mechanisms to clinical applications. Signal Transduction and Targeted Therapy, 8, 201. https://doi.org/10.1038/s41392-023-01406-7

 

Zhu, L., Gu, Q., & Fang, L. (2019). Cholesterol-mediated regulation of angiogenesis: An emerging paradigm. Cardiology Plus, 4, 1-9. DOI:10.4103/cp.cp_5_19

PDF
Full Text
Export Citation

View Dimensions


View Plumx



View Altmetric



27
Save
0
Citation
921
View
11
Share