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Review Articles

Targeting endothelial cell metabolism in cancerous microenvironment: a new approach for anti-angiogenic therapy

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon
Pages 386-400 | Received 06 Aug 2022, Accepted 18 Aug 2022, Published online: 27 Aug 2022

References

  • Aird WC. 2012. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med. 2(1):a006429.
  • Akella NM, Ciraku L, Reginato MJ. 2019. Fueling the fire: emerging role of the hexosamine biosynthetic pathway in cancer. BMC Biol. 17(1):52.
  • Ammazzalorso A, De Filippis B, Giampietro L, Amoroso R. 2017. N-acylsulfonamides: Synthetic routes and biological potential in medicinal chemistry. Chem Biol Drug Des. 90(6):1094–1105.
  • Annan DA, Maishi N, Soga T, Dawood R, Li C, Kikuchi H, Hojo T, Morimoto M, Kitamura T, Alam MT, et al. 2019. Carbonic anhydrase 2 (CAII) supports tumor blood endothelial cell survival under lactic acidosis in the tumor microenvironment. Cell Commun Signal. 17(1):169.
  • Baghban R, Roshangar L, Jahanban-Esfahlan R, Seidi K, Ebrahimi-Kalan A, Jaymand M, Kolahian S, Javaheri T, Zare P. 2020. Tumor microenvironment complexity and therapeutic implications at a glance. Cell Commun Signal. 18(1):59.
  • Boyd S, Brookfield JL, Critchlow SE, Cumming IA, Curtis NJ, Debreczeni J, Degorce SL, Donald C, Evans NJ, Groombridge S, et al. 2015. Structure-based design of potent and selective inhibitors of the metabolic kinase PFKFB3. J Med Chem. 58(8):3611–3625.
  • Brisson L, Bański P, Sboarina M, Dethier C, Danhier P, Fontenille M-J, Van Hée VF, Vazeille T, Tardy M, Falces J, et al. 2016. Lactate dehydrogenase B controls lysosome activity and autophagy in cancer. Cancer Cell. 30(3):418–431.
  • Bruning U, Morales-Rodriguez F, Kalucka J, Goveia J, Taverna F, Queiroz KCS, Dubois C, Cantelmo AR, Chen R, Loroch S, et al. 2018. Impairment of angiogenesis by fatty acid synthase inhibition involves mTOR malonylation. Cell Metab. 28(6):866–880.
  • Cantelmo AR, Conradi LC, Brajic A, Goveia J, Kalucka J, Pircher A, Chaturvedi P, Hol J, Thienpont B, Teuwen LA, et al. 2016. Inhibition of the glycolytic activator PFKFB3 in endothelium induces tumor vessel normalization, impairs metastasis, and improves chemotherapy. Cancer Cell. 30(6):968–985.
  • Chakraborty S, Njah K, Hong W. 2020. Agrin mediates angiogenesis in the tumor microenvironment. Trends Cancer. 6(2):81–85. eng.
  • Ciesielski O, Biesiekierska M, Panthu B, Vialichka V, Pirola L, Balcerczyk A. 2020. The epigenetic profile of tumor endothelial cells. effects of combined therapy with antiangiogenic and epigenetic drugs on cancer progression. IJMS. 21(7):2606.
  • Daghigh F, Fukuto JM, Ash DE. 1994. Inhibition of rat liver arginase by an intermediate in NO biosynthesis, NG-Hydroxy-L-arginine: implications for the regulation of nitric oxide biosynthesis by arginase. Biochem Biophys Res Commun. 202(1):174–180.
  • De Bock K, Georgiadou M, Schoors S, Kuchnio A, Wong BW, Cantelmo AR, Quaegebeur A, Ghesquiere B, Cauwenberghs S, Eelen G, et al. 2013. Role of PFKFB3-driven glycolysis in vessel sprouting. Cell. 154(3):651–663.
  • Draoui N, de Zeeuw P, Carmeliet P. 2017. Angiogenesis revisited from a metabolic perspective: role and therapeutic implications of endothelial cell metabolism. Open Biol. 7(12):170219.
  • Eelen G, de Zeeuw P, Simons M, Carmeliet P. 2015. Endothelial cell metabolism in normal and diseased vasculature. Circ Res. 116(7):1231–1244.
  • Eelen G, de Zeeuw P, Treps L, Harjes U, Wong BW, Carmeliet P. 2018. Endothelial cell metabolism. Physiol Rev. 98(1):3–58. eng.
  • Elice F, Rodeghiero F. 2012. Side effects of anti-angiogenic drugs. Thrombosis Research. 129:S50–S53.
  • Falkenberg KD, Rohlenova K, Luo Y, Carmeliet P. 2019. The metabolic engine of endothelial cells. Nat Metab. 1(10):937–946.
  • Fitzgerald G, Soro-Arnaiz I, De Bock K. 2018. The Warburg effect in endothelial cells and its potential as an anti-angiogenic target in cancer. Front Cell Dev Biol. 6:100.
  • Ghanbari Movahed Z, Rastegari-Pouyani M, Mohammadi M, Mansouri K. 2019. Cancer cells change their glucose metabolism to overcome increased ROS: one step from cancer cell to cancer stem cell? Biomed Pharmacother. 112:108690.
  • Ghinea N. 2021. Anti-angiogenic therapy: albumin-binding proteins could mediate mechanisms underlying the accumulation of small molecule receptor tyrosine kinase inhibitors in normal tissues with potential harmful effects on health. Diseases. 9(2):28.
  • Goveia J, Stapor P, Carmeliet P. 2014. Principles of targeting endothelial cell metabolism to treat angiogenesis and endothelial cell dysfunction in disease. EMBO Mol Med. 6(9):1105–1120.
  • Gross MI, Demo SD, Dennison JB, Chen L, Chernov-Rogan T, Goyal B, Janes JR, Laidig GJ, Lewis ER, Li JJ, et al. 2014. Antitumor activity of the glutaminase inhibitor CB-839 in triple-negative breast cancer. Mol Cancer Ther. 13(4):890–901.
  • Harjes U, Bensaad K, Harris AL. 2012. Endothelial cell metabolism and implications for cancer therapy. Br J Cancer. 107(8):1207–1212.
  • Heske CM. 2019. Beyond energy metabolism: exploiting the additional roles of NAMPT for cancer therapy. Front Oncol. 9:1514.
  • Hida K, Hida Y, Shindoh M. 2008. Understanding tumor endothelial cell abnormalities to develop ideal anti-angiogenic therapies. Cancer Sci. 99(3):459–466.
  • Iacovelli R, Palazzo A, Procopio G, Santoni M, Trenta P, De Benedetto A, Mezi S, Cortesi E. 2014. Incidence and relative risk of hepatic toxicity in patients treated with anti-angiogenic tyrosine kinase inhibitors for malignancy. Br J Clin Pharmacol. 77(6):929–938.
  • Ikeuchi H, Ahn Y-M, Otokawa T, Watanabe B, Hegazy L, Hiratake J, Richards N. 2012. A sulfoximine-based inhibitor of human asparagine synthetase kills L-asparaginase-resistant leukemia cells. Bioorg Med Chem. 20(19):5915–5927.
  • Jahani M, Noroznezhad F, Mansouri K. 2018. Arginine: challenges and opportunities of this two-faced molecule in cancer therapy. Biomed Pharmacother. 102:594–601.
  • Jahani M, Rezazadeh D, Mohammadi P, Abdolmaleki A, Norooznezhad A, Mansouri K. 2020. Regenerative medicine and angiogenesis; challenges and opportunities. Adv Pharm Bull. 10(4):490–501.
  • Jones W, Bianchi K. 2015. Aerobic glycolysis: beyond proliferation. Front Immunol. 6:227–227.
  • Kalucka J, Bierhansl L, Conchinha NV, Missiaen R, Elia I, Bruning U, Scheinok S, Treps L, Cantelmo AR, Dubois C, et al. 2018. Quiescent endothelial cells upregulate fatty acid beta-oxidation for vasculoprotection via redox homeostasis. Cell Metab. 28(6):881–894.
  • Kardideh B, Samimi Z, Norooznezhad F, Kiani S, Mansouri K. 2019. Autophagy, cancer and angiogenesis: where is the link? Cell Biosci. 9(1):65.
  • Kim B, Jang C, Dharaneeswaran H, Li J, Bhide M, Yang S, Li K, Arany Z. 2018. Endothelial pyruvate kinase M2 maintains vascular integrity. J Clin Investigation. 128:4543–4556.
  • Koroniak L, Ciustea M, Gutierrez JA, Richards NGJ. 2003. Synthesis and characterization of an N-Acylsulfonamide inhibitor of human asparagine synthetase. Org Lett. 5(12):2033–2036.
  • Li X, Kumar A, Carmeliet P. 2019. Metabolic pathways fueling the endothelial cell drive. Annu Rev Physiol. 81:483–503.
  • Li X, Sun X, Carmeliet P. 2019. Hallmarks of endothelial cell metabolism in health and disease. Cell Metab. 30(3):414–433.
  • Lin T-C. 2022. Updated functional roles of NAMPT in carcinogenesis and therapeutic niches. Cancers. 14(9):2059.
  • Lugano R, Ramachandran M, Dimberg A. 2020. Tumor angiogenesis: causes, consequences, challenges and opportunities. Cell Mol Life Sci. 77(9):1745–1770.
  • Lupo G, Caporarello N, Olivieri M, Cristaldi M, Motta C, Bramanti V, Avola R, Salmeri M, Nicoletti F, Anfuso CD. 2016. Anti-angiogenic therapy in cancer: downsides and new pivots for precision medicine. Front Pharmacol. 7:519.
  • Maishi N, Annan DA, Kikuchi H, Hida Y, Hida K. 2019. Tumor endothelial heterogeneity in cancer progression. Cancers. 11(10):1511.
  • Marcu R, Choi YJ, Xue J, Fortin CL, Wang Y, Nagao RJ, Xu J, MacDonald JW, Bammler TK, Murry CE, et al. 2018. Human organ-specific endothelial cell heterogeneity. iScience. 4:20–35.
  • Marcu R, Zheng Y, Hawkins BJ. 2017. Mitochondria and angiogenesis. Adv Exp Med Biol. 982:371–406.
  • Margadant C. 2020. Positive and negative feedback mechanisms controlling tip/stalk cell identity during sprouting angiogenesis. Angiogenesis. 23(2):75–77.
  • Mishra D, Banerjee D. 2019. Lactate dehydrogenases as metabolic links between tumor and stroma in the tumor microenvironment. Cancers. 11(6):750.
  • Novellasdemunt L, Bultot L, Manzano A, Ventura F, Rosa JL, Vertommen D, Rider MH, Navarro-Sabate A, Bartrons R. 2013. PFKFB3 activation in cancer cells by the p38/MK2 pathway in response to stress stimuli. Biochem J. 452(3):531–543.
  • Ohga N, Ishikawa S, Maishi N, Akiyama K, Hida Y, Kawamoto T, Sadamoto Y, Osawa T, Yamamoto K, Kondoh M, et al. 2012. Heterogeneity of tumor endothelial cells: comparison between tumor endothelial cells isolated from high- and low-metastatic tumors. Am J Pathol. 180(3):1294–1307.
  • Ohmura-Kakutani H, Akiyama K, Maishi N, Ohga N, Hida Y, Kawamoto T, Iida J, Shindoh M, Tsuchiya K, Shinohara N, et al. 2014. Identification of tumor endothelial cells with high aldehyde dehydrogenase activity and a highly angiogenic phenotype. PLoS One. 9(12):e113910.
  • Pasquier J, Ghiabi P, Chouchane L, Razzouk K, Rafii S, Rafii A. 2020. Angiocrine endothelium: from physiology to cancer. J Transl Med. 18(1):52.
  • Pedersen AK, Mendes Lopes de Melo J, Mørup N, Tritsaris K, Pedersen SF. 2017. Tumor microenvironment conditions alter Akt and Na+/H + exchanger NHE1 expression in endothelial cells more than hypoxia alone: implications for endothelial cell function in cancer. BMC Cancer. 17(1):542.
  • Peyton KJ, Liu XM, Yu Y, Yates B, Behnammanesh G, Durante W. 2018. Glutaminase-1 stimulates the proliferation, migration, and survival of human endothelial cells. Biochem Pharmacol. 156:204–214.
  • Pontes-Quero S, Fernández-Chacón M, Luo W, Lunella FF, Casquero-Garcia V, Garcia-Gonzalez I, Hermoso A, Rocha SF, Bansal M, Benedito R. 2019. High mitogenic stimulation arrests angiogenesis. Nat Commun. 10(1):2016.
  • Qin Z, Xiang C, Zhong F, Liu Y, Dong Q, Li K, Shi W, Ding C, Qin L, He F. 2019. Transketolase (TKT) activity and nuclear localization promote hepatocellular carcinoma in a metabolic and a non-metabolic manner. J Exp Clin Cancer Res. 38(1):154.
  • Rahimi N. 2019. Glycosylation in the tumor microenvironment: implications for tumor angiogenesis and metastasis.
  • Rajappa M, Saxena P, Kaur J. 2010. Chapter 6 – ocular angiogenesis: mechanisms and recent advances in therapy. In Makowski GS, editor. Advances in Clinical Chemistry. Amsterdam: Elsevier; p. 103–121.
  • Rao N, Lee YF, Ge R. 2015. Novel endogenous angiogenesis inhibitors and their therapeutic potential. Acta Pharmacol Sin. 36(10):1177–1190.
  • Rohlenova K, Veys K, Miranda-Santos I, De Bock K, Carmeliet P. 2018. Endothelial cell metabolism in health and disease. Trends Cell Biol. 28(3):224–236.
  • Schoonjans CA, Mathieu B, Joudiou N, Zampieri LX, Brusa D, Sonveaux P, Feron O, Gallez B. 2020. Targeting endothelial cell metabolism by inhibition of pyruvate dehydrogenase kinase and glutaminase-1. JCM. 9(10):3308.
  • Schoors S, De Bock K, Cantelmo AR, Georgiadou M, Ghesquiere B, Cauwenberghs S, Kuchnio A, Wong BW, Quaegebeur A, Goveia J, et al. 2014. Partial and transient reduction of glycolysis by PFKFB3 blockade reduces pathological angiogenesis. Cell Metab. 19(1):37–48.
  • Udupa S, Nguyen S, Hoang G, Nguyen T, Quinones A, Pham K, Asaka R, Nguyen K, Zhang C, Elgogary A, et al. 2019. Upregulation of the glutaminase II pathway contributes to glutamate production upon glutaminase 1 inhibition in pancreatic cancer. Proteomics. 19(21–22):e1800451.
  • van Beijnum JR, Dings RP, van der Linden E, Zwaans BM, Ramaekers FC, Mayo KH, Griffioen AW. 2006. Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood. 108(7):2339–2348.
  • Vandekeere S, Dewerchin M, Carmeliet P. 2015. Angiogenesis revisited: an overlooked role of endothelial cell metabolism in vessel sprouting. Microcirculation. 22(7):509–517.
  • Vandekeere S, Dubois C, Kalucka J, Sullivan MR, Garcia-Caballero M, Goveia J, Chen R, Diehl FF, Bar-Lev L, Souffreau J, et al. 2018. Serine synthesis via PHGDH is essential for heme production in endothelial cells. Cell Metab. 28(4):573–587.e513.
  • Verdegem D, Moens S, Stapor P, Carmeliet P. 2014. Endothelial cell metabolism: parallels and divergences with cancer cell metabolism. Cancer Metab. 2:19.
  • Wei X, Schneider JG, Shenouda SM, Lee A, Towler DA, Chakravarthy MV, Vita JA, Semenkovich CF. 2011. De novo lipogenesis maintains vascular homeostasis through endothelial nitric-oxide synthase (eNOS) palmitoylation. J Biol Chem. 286(4):2933–2945.
  • Yalcin A, Clem BF, Imbert-Fernandez Y, Ozcan SC, Peker S, O'Neal J, Klarer AC, Clem AL, Telang S, Chesney J. 2014. 6-Phosphofructo-2-kinase (PFKFB3) promotes cell cycle progression and suppresses apoptosis via Cdk1-mediated phosphorylation of p27. Cell Death Dis. 5:e1337.
  • Yalcin A, Clem BF, Simmons A, Lane A, Nelson K, Clem AL, Brock E, Siow D, Wattenberg B, Telang S, et al. 2009. Nuclear targeting of 6-phosphofructo-2-kinase (PFKFB3) increases proliferation via cyclin-dependent kinases. J Biol Chem. 284(36):24223–24232.
  • Yang Z, Ming X-F. 2013. Arginase: the emerging therapeutic target for vascular oxidative stress and inflammation. Front Immunol. 4:149–149.
  • Yetkin-Arik B, Vogels IMC, Nowak-Sliwinska P, Weiss A, Houtkooper RH, Van Noorden CJF, Klaassen I, Schlingemann RO. 2019. The role of glycolysis and mitochondrial respiration in the formation and functioning of endothelial tip cells during angiogenesis. Sci Rep. 9(1):12608.
  • Yoshida GJ. 2015. Metabolic reprogramming: the emerging concept and associated therapeutic strategies. J Exp Clin Cancer Res. 34:111.
  • Yu X, Li S. 2017. Non-metabolic functions of glycolytic enzymes in tumorigenesis. Oncogene. 36(19):2629–2636.
  • Zecchin A, Kalucka J, Dubois C, Carmeliet P. 2017. How endothelial cells adapt their metabolism to form vessels in tumors. Front Immunol. 8:1750.
  • Zhu L, Gu Q, Fang L. 2019. Cholesterol-mediated regulation of angiogenesis: an emerging paradigm. Cardiology Plus. 4(1):1–9.
  • Zhu W, Radadiya A, Bisson C, Wenzel S, Nordin BE, Martínez-Márquez F, Imasaki T, Sedelnikova SE, Coricello A, Baumann P, et al. 2019. High-resolution crystal structure of human asparagine synthetase enables analysis of inhibitor binding and selectivity. Commun Biol. 2(1):345.

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