Skip to main content
SpringerLink
Log in

Reciprocal Crosstalk Between Angiogenesis and Metabolism

  • Chapter
  • First Online:
Book cover Molecular Mechanisms of Angiogenesis

  • 1293 Accesses

Abstract

As the primary function of blood vessels is to transport the oxygen and the nutrients throughout the organism, it is not surprising that their formation is regulated by variation in oxygen and metabolic factors. The regulation of angiogenesis by oxygen concentration has been well described. However, metabolism in endothelial cells (ECs) and its effect on angiogenesis have only been recently characterized.

ECs are quiescent cells, which, upon stimulation by hypoxia or growth factors, rapidly switch to an active state and form new vessels Jakobsson et al. (2010). During vessel sprouting, ECs release enzymes to degrade the basement membrane, allowing them to escape from the parent vessel. Then an endothelial tip cell proliferates into the surrounding matrix followed by endothelial stalk cells that elongate the branch, whereas endothelial phalanx cells line quiescent perfused vessels. Tip and stalk cells can dynamically switch phenotypes under the control of vascular endothelial growth factor A (VEGF-A), a major proangiogenic growth factor, and Notch signaling (Jakobsson et al., Nat Cell Biol 12:943–953, 2010). Little is known about the different metabolic characteristics and requirements of these various EC subtypes and whether Notch controls metabolism in ECs. Recently, some studies characterized how some metabolic pathways regulate vessel sprouting.

In this chapter, we highlight emerging evidence demonstrating how, in addition to oxygen, regulation by metabolic intermediates and regulators dynamically shapes the vasculature. We will overview the current understanding of the various metabolic pathways in ECs and their impact on vessel formation. Finally, we will also address the effect of angiogenesis on metabolism.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Bibliography

  • Agani FH, Pichiule P, Chavez JC, LaManna JC (2000) The role of mitochondria in the regulation of hypoxia-inducible factor 1 expression during hypoxia. J Biol Chem 275:35863–35867

    Article  CAS  PubMed  Google Scholar 

  • Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, Deng CX, Finkel T (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A 105:14447–14452

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM et al (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451:1008–1012

    Article  CAS  PubMed  Google Scholar 

  • Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, Cohen C, Moses M, Kilroy S, Arnold RS et al (2002) Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci U S A 99:715–720

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barish GD, Narkar VA, Evans RM (2006) PPAR delta: a dagger in the heart of the metabolic syndrome. J Clin Invest 116:590–597

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barthel A, Schmoll D, Unterman TG (2005) FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab 16:183–189

    Article  CAS  PubMed  Google Scholar 

  • Bell EL, Guarente L (2011) The SirT3 divining rod points to oxidative stress. Mol Cell 42:561–568

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, Chandel NS (2007) The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 177:1029–1036

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bouloumie A, Lolmede K, Sengenes C, Galitzky J, Lafontan M (2002) Angiogenesis in adipose tissue. Ann Endocrinol (Paris) 63:91–95

    CAS  Google Scholar 

  • Brauchle M, Funk JO, Kind P, Werner S (1996) Ultraviolet B and H2O2 are potent inducers of vascular endothelial growth factor expression in cultured keratinocytes. J Biol Chem 271:21793–21797

    Article  CAS  PubMed  Google Scholar 

  • Brissova M, Shostak A, Shiota M, Wiebe PO, Poffenberger G, Kantz J, Chen Z, Carr C, Jerome WG, Chen J et al (2006) Pancreatic islet production of vascular endothelial growth factor–a is essential for islet vascularization, revascularization, and function. Diabetes 55:2974–2985

    Article  CAS  PubMed  Google Scholar 

  • Cao Y (2007) Angiogenesis modulates adipogenesis and obesity. J Clin Invest 117:2362–2368

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275:25130–25138

    Article  CAS  PubMed  Google Scholar 

  • Chen R, Dioum EM, Hogg RT, Gerard RD, Garcia JA (2011) Hypoxia increases sirtuin 1 expression in a hypoxia-inducible factor-dependent manner. J Biol Chem 286:13869–13878

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chinsomboon J, Ruas J, Gupta RK, Thom R, Shoag J, Rowe GC, Sawada N, Raghuram S, Arany Z (2009) The transcriptional coactivator PGC-1alpha mediates exercise-induced angiogenesis in skeletal muscle. Proc Natl Acad Sci U S A 106:21401–21406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Culic O, Gruwel ML, Schrader J (1997) Energy turnover of vascular endothelial cells. Am J Physiol 273:C205–C213

    CAS  PubMed  Google Scholar 

  • Dalgard CL, Lu H, Mohyeldin A, Verma A (2004) Endogenous 2-oxoacids differentially regulate expression of oxygen sensors. Biochem J 380:419–424

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Daly C, Wong V, Burova E, Wei Y, Zabski S, Griffiths J, Lai KM, Lin HC, Ioffe E, Yancopoulos GD et al (2004) Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev 18:1060–1071

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dang CV (2012) Links between metabolism and cancer. Genes Dev 26:877–890

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 154:651–663

    Article  PubMed  Google Scholar 

  • Diebold I, Flugel D, Becht S, Belaiba RS, Bonello S, Hess J, Kietzmann T, Gorlach A (2010) The hypoxia-inducible factor-2alpha is stabilized by oxidative stress involving NOX4. Antioxid Redox Signal 13:425–436

    Article  CAS  PubMed  Google Scholar 

  • Dioum EM, Chen R, Alexander MS, Zhang Q, Hogg RT, Gerard RD, Garcia JA (2009) Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science 324:1289–1293

    Article  CAS  PubMed  Google Scholar 

  • Duyndam MC, Hulscher TM, Fontijn D, Pinedo HM, Boven E (2001) Induction of vascular endothelial growth factor expression and hypoxia-inducible factor 1alpha protein by the oxidative stressor arsenite. J Biol Chem 276:48066–48076

    CAS  PubMed  Google Scholar 

  • Emerling BM, Platanias LC, Black E, Nebreda AR, Davis RJ, Chandel NS (2005) Mitochondrial reactive oxygen species activation of p38 mitogen-activated protein kinase is required for hypoxia signaling. Mol Cell Biol 25:4853–4862

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Enomoto N, Koshikawa N, Gassmann M, Hayashi J, Takenaga K (2002) Hypoxic induction of hypoxia-inducible factor-1alpha and oxygen-regulated gene expression in mitochondrial DNA-depleted HeLa cells. Biochem Biophys Res Commun 297:346–352

    Article  CAS  PubMed  Google Scholar 

  • Evans RM, Barish GD, Wang YX (2004) PPARs and the complex journey to obesity. Nat Med 10:355–361

    Article  CAS  PubMed  Google Scholar 

  • Fandrey J, Frede S, Jelkmann W (1994) Role of hydrogen peroxide in hypoxia-induced erythropoietin production. Biochem J 303(Pt 2):507–510

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fayard E, Xue G, Parcellier A, Bozulic L, Hemmings BA (2010) Protein kinase B (PKB/Akt), a key mediator of the PI3K signaling pathway. Curr Top Microbiol Immunol 346:31–56

    CAS  PubMed  Google Scholar 

  • Finck BN, Kelly DP (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest 116:615–622

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J, Teruya-Feldstein J, Moreira PI, Cardoso SM, Clish CB et al (2011) SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell 19:416–428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Formenti F, Constantin-Teodosiu D, Emmanuel Y, Cheeseman J, Dorrington KL, Edwards LM, Humphreys SM, Lappin TR, McMullin MF, McNamara CJ et al (2010) Regulation of human metabolism by hypoxia-inducible factor. Proc Natl Acad Sci U S A 107:12722–12727

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fukumura D, Ushiyama A, Duda DG, Xu L, Tam J, Krishna V, Chatterjee K, Garkavtsev I, Jain RK (2003) Paracrine regulation of angiogenesis and adipocyte differentiation during in vivo adipogenesis. Circ Res 93:e88–e97

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Furuyama T, Kitayama K, Shimoda Y, Ogawa M, Sone K, Yoshida-Araki K, Hisatsune H, Nishikawa S, Nakayama K, Ikeda K et al (2004) Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice. J Biol Chem 279:34741–34749

    Article  CAS  PubMed  Google Scholar 

  • Gerald D, Berra E, Frapart YM, Chan DA, Giaccia AJ, Mansuy D, Pouyssegur J, Yaniv M, Mechta-Grigoriou F (2004) JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell 118:781–794

    Article  CAS  PubMed  Google Scholar 

  • Gorlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP, Kietzmann T, Busse R (2001) Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: Role of the p22(phox)-containing NADPH oxidase. Circ Res 89:47–54

    Article  CAS  PubMed  Google Scholar 

  • Goyal P, Weissmann N, Grimminger F, Hegel C, Bader L, Rose F, Fink L, Ghofrani HA, Schermuly RT, Schmidt HH et al (2004) Upregulation of NAD(P)H oxidase 1 in hypoxia activates hypoxia-inducible factor 1 via increase in reactive oxygen species. Free Radic Biol Med 36:1279–1288

    Article  CAS  PubMed  Google Scholar 

  • Greer SN, Metcalf JL, Wang Y, Ohh M (2012) The updated biology of hypoxia-inducible factor. EMBO J 31:2448–2460

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hagberg CE, Falkevall A, Wang X, Larsson E, Huusko J, Nilsson I, van Meeteren LA, Samen E, Lu L, Vanwildemeersch M et al (2010) Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature 464:917–921

    Article  CAS  PubMed  Google Scholar 

  • Hagberg CE, Mehlem A, Falkevall A, Muhl L, Fam BC, Ortsater H, Scotney P, Nyqvist D, Samen E, Lu L et al (2012) Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes. Nature 490:426–430

    Article  CAS  PubMed  Google Scholar 

  • Hewitson KS, Lienard BM, McDonough MA, Clifton IJ, Butler D, Soares AS, Oldham NJ, McNeill LA, Schofield CJ (2007) Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates. J Biol Chem 282:3293–3301

    Article  CAS  PubMed  Google Scholar 

  • Hirschey MD, Shimazu T, Huang JY, Schwer B, Verdin E (2011) SIRT3 regulates mitochondrial protein acetylation and intermediary metabolism. Cold Spring Harb Symp Quant Biol 76:267–277

    Article  CAS  PubMed  Google Scholar 

  • Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13:225–238

    CAS  PubMed  Google Scholar 

  • Hutley LJ, Herington AC, Shurety W, Cheung C, Vesey DA, Cameron DP, Prins JB (2001) Human adipose tissue endothelial cells promote preadipocyte proliferation. Am J Physiol Endocrinol Metab 281:E1037–E1044

    CAS  PubMed  Google Scholar 

  • Isaacs JS, Jung YJ, Mole DR, Lee S, Torres-Cabala C, Chung YL, Merino M, Trepel J, Zbar B, Toro J et al (2005) HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 8:143–153

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, Rosewell I, Busse M, Thurston G, Medvinsky A et al (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12:943–953

    Article  CAS  PubMed  Google Scholar 

  • Jiang BH, Semenza GL, Bauer C, Marti HH (1996) Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol 271:C1172–C1180

    CAS  PubMed  Google Scholar 

  • Jiang BH, Zheng JZ, Leung SW, Roe R, Semenza GL (1997) Transactivation and inhibitory domains of hypoxia-inducible factor 1alpha. Modulation of transcriptional activity by oxygen tension. J Biol Chem 272:19253–19260

    Article  CAS  PubMed  Google Scholar 

  • Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393–402

    Article  CAS  PubMed  Google Scholar 

  • Karpanen T, Bry M, Ollila HM, Seppanen-Laakso T, Liimatta E, Leskinen H, Kivela R, Helkamaa T, Merentie M, Jeltsch M et al (2008) Overexpression of vascular endothelial growth factor-B in mouse heart alters cardiac lipid metabolism and induces myocardial hypertrophy. Circ Res 103:1018–1026

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W (1999) Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 103:1489–1498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kietzmann T, Gorlach A (2005) Reactive oxygen species in the control of hypoxia-inducible factor-mediated gene expression. Semin Cell Dev Biol 16:474–486

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD, van der Meer R, Nguyen P, Savage J, Owens KM et al (2010) SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17:41–52

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koivunen P, Hirsila M, Remes AM, Hassinen IE, Kivirikko KI, Myllyharju J (2007) Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 282:4524–4532

    Article  CAS  PubMed  Google Scholar 

  • Krutzfeldt A, Spahr R, Mertens S, Siegmund B, Piper HM (1990) Metabolism of exogenous substrates by coronary endothelial cells in culture. J Mol Cell Cardiol 22:1393–1404

    Article  CAS  PubMed  Google Scholar 

  • Lammert E, Cleaver O, Melton D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294:564–567

    Article  CAS  PubMed  Google Scholar 

  • Lammert E, Gu G, McLaughlin M, Brown D, Brekken R, Murtaugh LC, Gerber HP, Ferrara N, Melton DA (2003) Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 13:1070–1074

    Article  CAS  PubMed  Google Scholar 

  • Lando D, Gorman JJ, Whitelaw ML, Peet DJ (2003) Oxygen-dependent regulation of hypoxia-inducible factors by prolyl and asparaginyl hydroxylation. Eur J Biochem 270:781–790

    Article  CAS  PubMed  Google Scholar 

  • Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 16:1466–1471

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Laurent G, Solari F, Mateescu B, Karaca M, Castel J, Bourachot B, Magnan C, Billaud M, Mechta-Grigoriou F (2008) Oxidative stress contributes to aging by enhancing pancreatic angiogenesis and insulin signaling. Cell Metab 7:113–124

    Article  CAS  PubMed  Google Scholar 

  • Lefebvre P, Chinetti G, Fruchart JC, Staels B (2006) Sorting out the roles of PPAR alpha in energy metabolism and vascular homeostasis. J Clin Invest 116:571–580

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leone TC, Weinheimer CJ, Kelly DP (1999) A critical role for the peroxisome proliferator-activated receptor alpha (PPARalpha) in the cellular fasting response: the PPARalpha-null mouse as a model of fatty acid oxidation disorders. Proc Natl Acad Sci U S A 96:7473–7478

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol Cell 38:864–878

    Article  CAS  PubMed  Google Scholar 

  • Lombard DB, Tishkoff DX, Bao J (2011) Mitochondrial sirtuins in the regulation of mitochondrial activity and metabolic adaptation. Handb Exp Pharmacol 206:163–188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • MacKenzie ED, Selak MA, Tennant DA, Payne LJ, Crosby S, Frederiksen CM, Watson DG, Gottlieb E (2007) Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol 27:3282–3289

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mansfield KD, Guzy RD, Pan Y, Young RM, Cash TP, Schumacker PT, Simon MC (2005) Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab 1:393–399

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maranchie JK, Zhan Y (2005) Nox4 is critical for hypoxia-inducible factor 2-alpha transcriptional activity in von Hippel-Lindau-deficient renal cell carcinoma. Cancer Res 65:9190–9193

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Masson N, Singleton RS, Sekirnik R, Trudgian DC, Ambrose LJ, Miranda MX, Tian YM, Kessler BM, Schofield CJ, Ratcliffe PJ (2012) The FIH hydroxylase is a cellular peroxide sensor that modulates HIF transcriptional activity. EMBO Rep 13:251–257

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meissner M, Stein M, Urbich C, Reisinger K, Suske G, Staels B, Kaufmann R, Gille J (2004) PPARalpha activators inhibit vascular endothelial growth factor receptor-2 expression by repressing Sp1-dependent DNA binding and transactivation. Circ Res 94:324–332

    Article  CAS  PubMed  Google Scholar 

  • Muller-Brusselbach S, Komhoff M, Rieck M, Meissner W, Kaddatz K, Adamkiewicz J, Keil B, Klose KJ, Moll R, Burdick AD et al (2007) Deregulation of tumor angiogenesis and blockade of tumor growth in PPARbeta-deficient mice. EMBO J 26:3686–3698

    Article  PubMed Central  PubMed  Google Scholar 

  • Ouchi N, Shibata R, Walsh K (2005) AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ Res 96:838–846

    Article  CAS  PubMed  Google Scholar 

  • Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z, Miao L, Tothova Z, Horner JW, Carrasco DR et al (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128:309–323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Panigrahy D, Kaipainen A, Huang S, Butterfield CE, Barnes CM, Fannon M, Laforme AM, Chaponis DM, Folkman J, Kieran MW (2008) PPARalpha agonist fenofibrate suppresses tumor growth through direct and indirect angiogenesis inhibition. Proc Natl Acad Sci U S A 105:985–990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Panigrahy D, Singer S, Shen LQ, Butterfield CE, Freedman DA, Chen EJ, Moses MA, Kilroy S, Duensing S, Fletcher C et al (2002) PPARgamma ligands inhibit primary tumor growth and metastasis by inhibiting angiogenesis. J Clin Invest 110:923–932

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parra-Bonilla G, Alvarez DF, Al-Mehdi AB, Alexeyev M, Stevens T (2010) Critical role for lactate dehydrogenase A in aerobic glycolysis that sustains pulmonary microvascular endothelial cell proliferation. Am J Physiol Lung Cell Mol Physiol 299:L513–L522

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Piqueras L, Reynolds AR, Hodivala-Dilke KM, Alfranca A, Redondo JM, Hatae T, Tanabe T, Warner TD, Bishop-Bailey D (2007) Activation of PPARbeta/delta induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol 27:63–69

    Article  CAS  PubMed  Google Scholar 

  • Potente M, Urbich C, Sasaki K, Hofmann WK, Heeschen C, Aicher A, Kollipara R, DePinho RA, Zeiher AM, Dimmeler S (2005) Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 115:2382–2392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pouyssegur J, Dayan F, Mazure NM (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437–443

    Article  CAS  PubMed  Google Scholar 

  • Pouyssegur J, Mechta-Grigoriou F (2006) Redox regulation of the hypoxia-inducible factor. Biol Chem 387:1337–1346

    Article  CAS  PubMed  Google Scholar 

  • Qiu X, Brown K, Hirschey MD, Verdin E, Chen D (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12:662–667

    Article  CAS  PubMed  Google Scholar 

  • Ratcliffe PJ (2013) Oxygen sensing and hypoxia signalling pathways in animals: the implications of physiology for cancer. J Physiol 591:2027–2042

    CAS  PubMed Central  PubMed  Google Scholar 

  • Safran M, Kaelin WG Jr (2003) HIF hydroxylation and the mammalian oxygen-sensing pathway. J Clin Invest 111:779–783

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5:343–354

    Article  CAS  PubMed  Google Scholar 

  • Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, Pan Y, Simon MC, Thompson CB, Gottlieb E (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7:77–85

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3:721–732

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2007) Life with oxygen. Science 318:62–64

    Article  CAS  PubMed  Google Scholar 

  • Srinivas V, Leshchinsky I, Sang N, Kng MP, Minchenko A, Caro J (2001) Oxygen sensing and HIF-1 activation does not require an active mitochondrial respiratory chain electron-transfer pathway. J Biol Chem 276:21995–21998

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi CM, Finger EC, Krieg AJ, Wu C, Diep AN, Lagory EL, Wei K, McGinnis LM, Yuan J, Kuo CJ, Giaccia AJ et al (2013) Cross-talk between hypoxia and insulin signaling through Phd3 regulates hepatic glucose and lipid metabolism and ameliorates diabetes. Nature Med 19:1325–1330

    Google Scholar 

  • Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H, Kim HS, Flynn CR, Hill S, Hayes McDonald W et al (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40:893–904

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tormos KV, Chandel NS (2010) Inter-connection between mitochondria and HIFs. J Cell Mol Med 14:795–804

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Toullec A, Gerald D, Despouy G, Bourachot B, Cardon M, Lefort S, Richardson M, Rigaill G, Parrini MC, Lucchesi C et al (2010) Oxidative stress promotes myofibroblast differentiation and tumour spreading. EMBO Mol Med 2:211–230

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tzivion G, Dobson M, Ramakrishnan G (2011) FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta 1813:1938–1945

    Article  CAS  PubMed  Google Scholar 

  • Varzaneh FE, Shillabeer G, Wong KL, Lau DC (1994) Extracellular matrix components secreted by microvascular endothelial cells stimulate preadipocyte differentiation in vitro. Metabolism 43:906–912

    Article  CAS  PubMed  Google Scholar 

  • Vaux EC, Metzen E, Yeates KM, Ratcliffe PJ (2001) Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 98:296–302

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Wang H, Guo Y, Ning W, Katkuri S, Wahli W, Desvergne B, Dey SK, DuBois RN (2006) Crosstalk between peroxisome proliferator-activated receptor delta and VEGF stimulates cancer progression. Proc Natl Acad Sci U S A 103:19069–19074

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weidemann A, Johnson RS (2008) Biology of HIF-1alpha. Cell Death Differ 15:621–627

    Article  CAS  PubMed  Google Scholar 

  • Wright GL, Maroulakou IG, Eldridge J, Liby TL, Sridharan V, Tsichlis PN, Muise-Helmericks RC (2008) VEGF stimulation of mitochondrial biogenesis: requirement of AKT3 kinase. FASEB J 22:3264–3275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong L, D’Urso A, Toiber D, Sebastian C, Henry RE, Vadysirisack DD, Guimaraes A, Marinelli B, Wikstrom JD, Nir T et al (2010) The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140:280–293

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell Biology, Harvard Medical School, Boston, USA

    Gaëlle Laurent

  2. Stress and Cancer Laboratory, Institut Curie, 26, rue d’Ulm, Paris, 75248, France

    Fatima Mechta-Grigoriou

  3. Inserm U830, Paris, F-75248, France

    Fatima Mechta-Grigoriou

Authors
  1. Gaëlle Laurent
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatima Mechta-Grigoriou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatima Mechta-Grigoriou .

Editor information

Editors and Affiliations

  1. UMR 1036, Biologie du Cancer et de l’Infection, Institut de Recherches en Technologies et Sciences pour le Vivant, Université Grenoble-Alpes, Grenoble, France

    Jean-Jacques Feige

  2. Institute for Research on Cancer and aging of Nice (IRCAN), University of Nice Sophia Antipolis, Nice, France

    Gilles Pagès

  3. CNRS UMR8161, Institut Pasteur de Lille, Institut de Biologie de Lille, Lille, France

    Fabrice Soncin

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag France

About this chapter

Cite this chapter

Laurent, G., Mechta-Grigoriou, F. (2014). Reciprocal Crosstalk Between Angiogenesis and Metabolism. In: Feige, JJ., Pagès, G., Soncin, F. (eds) Molecular Mechanisms of Angiogenesis. Springer, Paris. https://doi.org/10.1007/978-2-8178-0466-8_10

Download citation

Publish with us

Policies and ethics

Search

Navigation