Endothelial PFKFB3 plays a critical role in angiogenesis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 6, 2014, Pages 1231-1239

  Xu, Yiming ^a   An, Xiaofei ^a,b   Guo, Xin ^c   Habtetsion, Tsadik Ghebreamlak ^a   Wang, Yong ^a   Xu, Xizhen ^a   Kandala, Sridhar ^a   Li, Qinkai ^b   Li, Honggui ^c   Zhang, Chunxiang ^d   Caldwell, Ruth B ^a   Fulton, David J ^a   Su, Yunchao ^a   Hoda, Md Nasrul ^a   Zhou, Gang ^a   Wu, Chaodong ^c   Huo, Yuqing ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b PEKING UNIVERSITY   (China)

^c TEXAS A AND M UNIVERSITY   (United States)

^d RUSH MEDICAL COLLEGE   (United States)

Author keywords

angiogenesis; anoxia; endothelial cells; glycolysis

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE FRUCTOSE 2,6 BISPHOSPHATASE ISOFORM 3 INHIBITOR; ANGIOGENIC FACTOR; ENZYME INHIBITOR; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; ENDOTHELIUM CELL; FEMALE; GENE DELETION; GENE OVEREXPRESSION; GLYCOLYSIS; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; OXYGEN-INDUCED RETINOPATHY; PRIORITY JOURNAL; RETINA NEOVASCULARIZATION; UPREGULATION; VASCULARIZATION;

ANGIOGENESIS; ANOXIA; ENDOTHELIAL CELLS; GLYCOLYSIS;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; GLYCOLYSIS; HUMANS; LACTIC ACID; MALE; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHOFRUCTOKINASE-2; PROTO-ONCOGENE PROTEINS C-AKT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84901482495     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.303041     Document Type: Article

References (36)

1. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653-660. (Pubitemid 36749213)
2. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell. 2011;146:873-887.
3. Eilken HM, Adams RH. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol. 2010;22:617-625.
4. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature. 2011;473:298-307.
5. De Bock K, Georgiadou M, Carmeliet P. Role of endothelial cell metabolism in vessel sprouting. Cell Metab. 2013;18:634-647.
6. De Bock K, Georgiadou M, Schoors S, et al. Role of PFKFB3-driven glycolysis in vessel sprouting. Cell. 2013;154:651-663.
7. Merchan JR, Kovács K, Railsback JW, Kurtoglu M, Jing Y, Piña Y, Gao N, Murray TG, Lehrman MA, Lampidis TJ. Antiangiogenic activity of 2-deoxy-D-glucose. PLoS One. 2010;5:e13699.
8. Quintero M, Colombo SL, Godfrey A, Moncada S. Mitochondria as signaling organelles in the vascular endothelium. Proc Natl Acad Sci U S A. 2006;103:5379-5384.
9. Davidson SM, Duchen MR. Endothelial mitochondria: contributing to vascular function and disease. Circ Res. 2007;100:1128-1141. (Pubitemid 46684126)
10. Ros S, Schulze A. Balancing glycolytic flux: the role of 6- phosphofructo-2-kinase/fructose 2,6-bisphosphatases in cancer metabolism. Cancer Metab. 2013;1:8.
11. Bando H, Atsumi T, Nishio T, Niwa H, Mishima S, Shimizu C, Yoshioka N, Bucala R, Koike T. Phosphorylation of the 6- phosphofructo-2-kinase/fructose 2,6-bisphosphatase/PFKFB3 family of glycolytic regulators in human cancer. Clin Cancer Res. 2005;11:5784-5792. (Pubitemid 41170304)
12. Clem B, Telang S, Clem A, Yalcin A, Meier J, Simmons A, Rasku MA, Arumugam S, Dean WL, Eaton J, Lane A, Trent JO, Chesney J. Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth. Mol Cancer Ther. 2008;7:110-120.
13. Guo X, Li H, Xu H, Halim V, Thomas LN, Woo SL, Huo Y, Chen YE, Sturino JM, Wu C. Disruption of inducible 6-phosphofructo-2-kinase impairs the suppressive effect of ppargamma activation on diet-induced intestine inflammatory response. J Nutr Biochem. 2013;24:770-775.
14. Guo X, Xu K, Zhang J, Li H, Zhang W, Wang H, Lange AJ, Chen YE, Huo Y, Wu C. Involvement of inducible 6-phosphofructo-2-kinase in the anti-diabetic effect of peroxisome proliferator-activated receptor gamma activation in mice. J Biol Chem. 2010;285:23711-23720.
15. Huo Y, Guo X, Li H, Wang H, Zhang W, Wang Y, Zhou H, Gao Z, Telang S, Chesney J, Chen YE, Ye J, Chapkin RS, Wu C. Disruption of inducible 6-phosphofructo-2-kinase ameliorates diet-induced adiposity but exacerbates systemic insulin resistance and adipose tissue inflammatory response. J Biol Chem. 2010;285:3713-3721.
16. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, Shibata R, Ouchi N, Easton RM, Galasso G, Birnbaum MJ, Walsh K, Sessa WC. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest. 2005;115:2119-2127. (Pubitemid 41134153)
17. Chen J, Somanath PR, Razorenova O, Chen WS, Hay N, Bornstein P, Byzova TV. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat Med. 2005;11:1188-1196. (Pubitemid 43093666)
18. Bolaños JP. Adapting glycolysis to cancer cell proliferation: the MAPK pathway focuses on PFKFB3. Biochem J. 2013;452:e7-e9.
19. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol. 2011;27:441-464.
20. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029-1033.
21. Colombo SL, Palacios-Callender M, Frakich N, De Leon J, Schmitt CA, Boorn L, Davis N, Moncada S. Anaphase-promoting complex/cyclosome-Cdh1 coordinates glycolysis and glutaminolysis with transition to S phase in human T lymphocytes. Proc Natl Acad Sci U S A. 2010;107:18868-18873.
22. Tudzarova S, Colombo SL, Stoeber K, Carcamo S, Williams GH, Moncada S. Two ubiquitin ligases, APC/C-Cdh1 and SKP1-CUL1-F (SCF)-beta-TrCP, sequentially regulate glycolysis during the cell cycle. Proc Natl Acad Sci U S A. 2011;108:5278-5283.
23. Yalcin A, Clem BF, Simmons A, Lane A, Nelson K, Clem AL, Brock E, Siow D, Wattenberg B, Telang S, Chesney J. Nuclear targeting of 6- phosphofructo-2- kinase (PFKFB3) increases proliferation via cyclin-dependent kinases. J Biol Chem. 2009;284:24223-24232.
24. Hunt TK, Aslam RS, Beckert S, Wagner S, Ghani QP, Hussain MZ, Roy S, Sen CK. Aerobically derived lactate stimulates revascularization and tissue repair via redox mechanisms. Antioxid Redox Signal. 2007;9:1115-1124. (Pubitemid 47080823)
25. Parra-Bonilla G, Alvarez DF, Alexeyev M, Vasauskas A, Stevens T. Lactate dehydrogenase a expression is necessary to sustain rapid angiogenesis of pulmonary microvascular endothelium. PLoS One. 2013;8:e75984.
26. Parra-Bonilla G, Alvarez DF, Al-Mehdi AB, Alexeyev M, Stevens T. Critical role for lactate dehydrogenase A in aerobic glycolysis that sustains pulmonary microvascular endothelial cell proliferation. Am J Physiol Lung Cell Mol Physiol. 2010;299:L513-L522.
27. Porporato PE, Payen VL, De Saedeleer CJ, Préat V, Thissen JP, Feron O, Sonveaux P. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis. 2012;15:581-592.
28. Ruan GX, Kazlauskas A. Lactate engages receptor tyrosine kinases Axl, Tie2, and vascular endothelial growth factor receptor 2 to activate phosphoinositide 3-kinase/Akt and promote angiogenesis. J Biol Chem. 2013;288:21161-21172.
29. Vegran F, Boidot R, Michiels C, Sonveaux P, Feron O. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κb/IL-8 pathway that drives tumor angiogenesis. Cancer Res. 2011;71:2550-2560.
30. Potente M, Urbich C, Sasaki K, Hofmann WK, Heeschen C, Aicher A, Kollipara R, De Pinho RA, Zeiher AM, Dimmeler S. Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest. 2005;115:2382-2392. (Pubitemid 41266200)
31. Zippo A, De Robertis A, Bardelli M, Galvagni F, Oliviero S. Identification of Flk-1 target genes in vasculogenesis: Pim-1 is required for endothelial and mural cell differentiation in vitro. Blood. 2004;103:4536-4544. (Pubitemid 38745981)
32. Katare R, Oikawa A, Cesselli D, Beltrami AP, Avolio E, Muthukrishnan D, Munasinghe PE, Angelini G, Emanueli C, Madeddu P. Boosting the pentose phosphate pathway restores cardiac progenitor cell availability in diabetes. Cardiovasc Res. 2013;97:55-65.
33. Leopold JA, Walker J, Scribner AW, Voetsch B, Zhang YY, Loscalzo AJ, Stanton RC, Loscalzo J. Glucose-6-phosphate dehydrogenase modulates vascular endothelial growth factor-mediated angiogenesis. J Biol Chem. 2003;278:32100-32106. (Pubitemid 37048399)
34. Schoors S, De Bock K, Cantelmo AR, et al. Partial and transient reduction of glycolysis by PFKFB3 blockade reduces pathological angiogenesis. Cell Metab. 2014;19:37-48.
35. Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov. 2011;10:417-427.
36. Herrmann J, Lerman LO, Mukhopadhyay D, Napoli C, Lerman A. Angiogenesis in atherogenesis. Arterioscler Thromb Vasc Biol. 2006;26:1948-1957. (Pubitemid 44253775)