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Abstract:

In the last years, several reports have established the notion that metabolism is not just a housekeeping process, but instead an active effector of physiological changes. The idea that the metabolic status may rule a wide range of phenomena in cell biology is starting to be broadly accepted. Thus, current developmental biology has begun to describe different ways by which the metabolic profile of the cell and developmental programs of the organism can crosstalk. In this review, we discuss mechanisms by which metabolism impacts on processes governing development. We review the growing body of evidence that supports the notion that aerobic glycolysis is required in cells undergoing fast growth and high proliferation, similarly to the Warburg effect described in tumor cells. Glycolytic metabolism explains not only the higher ATP synthesis rate required for cell growth, but also the uncoupling between mitochondrial activity and bioenergetics needed to provide anabolism with sufficient precursors. We also discuss some recent studies, which show that in addition to its role in providing energy and carbon chains, the metabolic status of the cell can also influence epigenetic regulation of developmental processes. Although metabolic aspects of development are just starting to be explored, there is no doubt that ongoing research in this field will shape the future landscape of Developmental Biology. © 2018 Elsevier B.V.

Registro:

Documento: Artículo
Título:Metabo-Devo: A metabolic perspective of development
Autor:Gándara, L.; Wappner, P.
Filiación:Instituto Leloir, Av. Patricias Argentinas 435, Ciudad de Buenos Aires, C1405BWE, Argentina
Departamento de Fisiología, Biología Molecular, y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Bioenergetics; Cell differentiation; Metabolism; Warburg effect; adenosine triphosphate; glucose transporter 1; glucose transporter 2; hexokinase; hexokinase 2; lactate dehydrogenase; lactate dehydrogenase A; lactate dehydrogenase C; pyruvate kinase; pyruvate kinase M2; unclassified drug; aerobic glycolysis; biomass; cancer cell; cell differentiation; cell energy; cell growth; cell migration; cell proliferation; developmental biology; developmental stage; DNA demethylation; Drosophila; ectoderm; embryo development; gene expression; genetic transcription; hematopoiesis; histone methylation; mitochondrion; mitophagy; nervous system development; nonhuman; oxidative phosphorylation; oxygen consumption; pluripotent stem cell; priority journal; protein synthesis; retina development; Review; tissue growth
Año:2018
Volumen:154
Página de inicio:12
Página de fin:23
DOI: http://dx.doi.org/10.1016/j.mod.2018.02.004
Título revista:Mechanisms of Development
Título revista abreviado:Mech. Dev.
ISSN:09254773
CODEN:MEDVE
CAS:adenosine triphosphate, 15237-44-2, 56-65-5, 987-65-5; glucose transporter 1, 172077-08-6; glucose transporter 2, 357693-20-0; hexokinase, 9001-51-8; lactate dehydrogenase, 9001-60-9; pyruvate kinase, 9001-59-6
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09254773_v154_n_p12_Gandara

Referencias:

  • Agathocleous, M., Harris, W.A., Metabolism in physiological cell proliferation and differentiation (2013) Trends Cell Biol., 23, pp. 484-492
  • Agathocleous, M., Love, N.K., Randlett, O., Harris, J.J., Liu, J., Murray, A.J., Harris, W.A., Metabolic differentiation in retinal cells (2012) Nat. Cell Biol., 14, p. 859
  • Agostini, M., Romeo, F., Inoue, S., Niklison-Chirou, M., Elia, A., Dinsdale, D., Morone, N., Melino, G., Metabolic reprogramming during neuronal differentiation (2016) Cell Death Differ., 23, p. 1502
  • Alaynick, W.A., Kondo, R.P., Xie, W., He, W., Dufour, C.R., Downes, M., Jonker, J.W., Giguere, V., ERRγ directs and maintains the transition to oxidative metabolism in the postnatal heart (2007) Cell Metab., 6, pp. 13-24
  • Allen, J.P., Biophysical Chemistry (2008), Blackwell Publishing; Anastasiou, D., Yu, Y., Israelsen, W.J., Jiang, J.-K., Boxer, M.B., Hong, B.S., Tempel, W., Jha, A., Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis (2012) Nat. Chem. Biol., 8, p. 839
  • Araldi, E., Schipani, E., Hypoxia, HIFs and bone development (2010) Bone, 47, pp. 190-196
  • Baek, G., Yan, F.T., Hu, Z., Cox, D., Buboltz, N., McCue, P., Yeo, C.J., Knudsen, E.S., MCT4 defines a glycolytic subtype of pancreatic cancer with poor prognosis and unique metabolic dependencies (2014) Cell Rep., 9, pp. 2233-2249
  • Baumann, M., Kappl, A., Lang, T., Brand, K., Siegfried, W., Paterok, E., The diagnostic validity of the serum tumor marker phosphohexose isomerase (PHI) in patients with gastrointestinal, kidney, and breast cancer (1990) Cancer Investig., 8, pp. 351-356
  • Beckmann, B.M., Horos, R., Fischer, B., Castello, A., Eichelbaum, K., Alleaume, A.-M., Schwarzl, T., Huber, W., The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs (2015) Nat. Commun., 6
  • Brand, K.A., Hermfisse, U., Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species (1997) FASEB J., 11, pp. 388-395
  • Bricker, D.K., Taylor, E.B., Schell, J.C., Orsak, T., Boutron, A., Chen, Y.-C., Cox, J.E., Dephoure, N., A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans (2012) Science, 337, pp. 96-100
  • Bulusu, V., Prior, N., Snaebjornsson, M.T., Kuehne, A., Sonnen, K.F., Kress, J., Stein, F., Aulehla, A., Spatiotemporal analysis of a glycolytic activity gradient linked to mouse embryo mesoderm development (2017) Dev. Cell, 40, pp. 331-341. , (e4)
  • Castello, A., Hentze, M.W., Preiss, T., Metabolic enzymes enjoying new partnerships as RNA-binding proteins (2015) Trends Endocrinol. Metab., 26, pp. 746-757
  • Chang, C.-H., Curtis, J.D., Maggi, L.B., Faubert, B., Villarino, A.V., O'Sullivan, D., Huang, S.C.-C., Qiu, J., Posttranscriptional control of T cell effector function by aerobic glycolysis (2013) Cell, 153, pp. 1239-1251
  • Chiang, E.-P.I., Wang, Y.-C., Chen, W.-W., Tang, F.-Y., Effects of insulin and glucose on cellular metabolic fluxes in homocysteine transsulfuration, remethylation, S‑adenosylmethionine synthesis, and global deoxyribonucleic acid methylation (2009) J. Clin. Endocrinol. Metab., 94, pp. 1017-1025
  • Christofk, H.R., Vander Heiden, M.G., Harris, M.H., Ramanathan, A., Gerszten, R.E., Wei, R., Fleming, M.D., Cantley, L.C., The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth (2008) Nature, 452, p. 230
  • Clough, J., Whittingham, D., Metabolism of [14C] glucose by postimplantation mouse embryos in vitro (1983) Development, 74, pp. 133-142
  • Crabtree, H.G., Observations on the carbohydrate metabolism of tumours (1929) Biochem. J., 23, p. 536
  • Dang, L., White, D.W., Gross, S., Bennett, B.D., Bittinger, M.A., Driggers, E.M., Fantin, V.R., Keenan, M.C., Cancer-associated IDH1 mutations produce 2‑hydroxyglutarate (2009) Nature, 462, p. 739
  • DeBerardinis, R.J., Lum, J.J., Hatzivassiliou, G., Thompson, C.B., The biology of cancer: metabolic reprogramming fuels cell growth and proliferation (2008) Cell Metab., 7, pp. 11-20
  • Desai, S., Ding, M., Wang, B., Lu, Z., Zhao, Q., Shaw, K., Yung, W.A., Yao, J., Tissue-specific isoform switch and DNA hypomethylation of the pyruvate kinase PKM gene in human cancers (2014) Oncotarget, 5, p. 8202
  • Esteban-Martínez, L., Sierra-Filardi, E., McGreal, R.S., Salazar-Roa, M., Mariño, G., Seco, E., Durand, S., Malumbres, M., Programmed mitophagy is essential for the glycolytic switch during cell differentiation (2017) EMBO J., 36, pp. 1688-1706
  • Fernández-Hernández, I., Rhiner, C., Moreno, E., Adult neurogenesis in Drosophila (2013) Cell Rep., 3, pp. 1857-1865
  • Feynman, R.P., Leighton, R.B., Sands, M., The Feynman lectures on physics (2011) The New Millennium Edition: Mainly Mechanics, Radiation, and Heat, Basic Books, I
  • Figueiredo, A.L., Maczkowiak, F., Borday, C., Pla, P., Sittewelle, M., Pegoraro, C., Monsoro-Burq, A.H., PFKFB4 control of AKT signaling is essential for premigratory and migratory neural crest formation (2017) Development, 144 (22), pp. 4183-4194
  • Filella, X., Molina, R., Jo, J., Mas, E., Ballesta, A., Serum phosphohexose isomerase activities in patients with colorectal cancer (1991) Tumor Biol., 12, pp. 360-367
  • Forni, M.F., Peloggia, J., Trudeau, K., Shirihai, O., Kowaltowski, A.J., Murine mesenchymal stem cell commitment to differentiation is regulated by mitochondrial dynamics (2016) Stem Cells, 34, pp. 743-755
  • Gatenby, R.A., Gillies, R.J., Why do cancers have high aerobic glycolysis? (2004) Nat. Rev. Cancer, 4, pp. 891-899
  • Gomez, C., Özbudak, E.M., Wunderlich, J., Baumann, D., Lewis, J., Pourquié, O., Control of segment number in vertebrate embryos (2008) Nature, 454, pp. 335-339
  • Gould, S.J., Darwinism and the expansion of evolutionary theory (1982) Science, 216, pp. 380-387
  • Gurdon, J.B., The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles (1962) Development, 10, pp. 622-640
  • Haeckel, E., Generelle Morphologie der Organismen allgemeine Grundzuge der organischen Formen-Wissenschaft, mechanisch begrundet durch die von Charles Darwin reformirte Descendenz-Theorie von Ernst Haeckel: Allgemeine Entwickelungsgeschichte der Organismen kritische Grundzuge der mechanischen Wissenschaft von den entstehenden Formen der Organismen, begrundet durch die Descendenz-Theorie, Verlag von Georg Reimer (1866); Hensley, C.T., Wasti, A.T., DeBerardinis, R.J., Glutamine and cancer: cell biology, physiology, and clinical opportunities (2013) J. Clin. Invest., 123, p. 3678
  • Hitosugi, T., Fan, J., Chung, T.-W., Lythgoe, K., Wang, X., Xie, J., Ge, Q., Roesel, J.L., Tyrosine phosphorylation of mitochondrial pyruvate dehydrogenase kinase 1 is important for cancer metabolism (2011) Mol. Cell, 44, pp. 864-877
  • Holness, M., Sugden, M., Regulation of Pyruvate Dehydrogenase Complex Activity by Reversible Phosphorylation (2003), Portland Press Limited; Homem, C.C., Steinmann, V., Burkard, T.R., Jais, A., Esterbauer, H., Knoblich, J.A., Ecdysone and mediator change energy metabolism to terminate proliferation in Drosophila neural stem cells (2014) Cell, 158, pp. 874-888
  • Horder, T., History of Developmental Biology (2001), eLS. John Wiley & Sons, Ltd; Ito, K., Hotta, Y., Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster (1992) Dev. Biol., 149, pp. 134-148
  • Jornayvaz, F.R., Shulman, G.I., Regulation of mitochondrial biogenesis (2010) Essays Biochem., 47, pp. 69-84
  • Kaplon, J., Zheng, L., Meissl, K., Chaneton, B., Selivanov, V.A., Mackay, G., van der Burg, S.H., Shlomi, T., A key role for mitochondrial gatekeeper pyruvate dehydrogenase in oncogene-induced senescence (2013) Nature, 498, p. 109
  • Kessler, R., Bleichert, F., Warnke, J.-P., Eschrich, K., 6‑Phosphofructo‑2‑kinase/fructose‑2, 6‑bisphosphatase (PFKFB3) is up-regulated in high-grade astrocytomas (2008) J. Neuro-Oncol., 86, pp. 257-264
  • Lee, D.C., Sohn, H.A., Park, Z.-Y., Oh, S., Kang, Y.K., Lee, K.-M., Kang, M., Hong, Y.K., A lactate-induced response to hypoxia (2015) Cell, 161, pp. 595-609
  • Li, H., Chawla, G., Hurlburt, A.J., Sterrett, M.C., Zaslaver, O., Cox, J., Karty, J.A., Tennessen, J.M., Drosophila larvae synthesize the putative oncometabolite L‑2‑hydroxyglutarate during normal developmental growth (2017) Proc. Natl. Acad. Sci., 201614102
  • Liu, J., Kim, J., Oberdoerffer, P., Metabolic modulation of chromatin: implications for DNA repair and genomic integrity (2013) Front. Genet., 4, p. 182
  • Loenarz, C., Schofield, C.J., Expanding chemical biology of 2‑oxoglutarate oxygenases (2008) Nat. Chem. Biol., 4, pp. 152-156
  • Martinez-Pastor, B., Cosentino, C., Mostoslavsky, R., A tale of metabolites: the cross-talk between chromatin and energy metabolism (2013) Cancer Discov., 3, pp. 497-501
  • Mathupala, S., Ko, Y.A., Pedersen, P., Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria (2006) Oncogene, 25, p. 4777
  • Medina, R.A., Owen, G.I., Glucose transporters: expression, regulation and cancer (2002) Biol. Res., 35, pp. 9-26
  • Melcer, S., Hezroni, H., Rand, E., Nissim-Rafinia, M., Skoultchi, A., Stewart, C.L., Bustin, M., Meshorer, E., Histone modifications and lamin A regulate chromatin protein dynamics in early embryonic stem cell differentiation (2012) Nat. Commun., 3, p. 910
  • Miao, P., Sheng, S., Sun, X., Liu, J., Huang, G., Lactate dehydrogenase A in cancer: a promising target for diagnosis and therapy (2013) IUBMB Life, 65, pp. 904-910
  • Minchenko, O., Ochiai, A., Opentanova, I., Ogura, T., Minchenko, D., Caro, J., Komisarenko, S., Esumi, H., Overexpression of 6‑phosphofructo‑2‑kinase/fructose‑2, 6‑bisphosphatase‑4 in the human breast and colon malignant tumors (2005) Biochimie, 87, pp. 1005-1010
  • Miyazawa, H., Yamaguchi, Y., Sugiura, Y., Honda, K., Kondo, K., Matsuda, F., Yamamoto, T., Miura, M., Rewiring of embryonic glucose metabolism via suppression of PFK-1 and aldolase during mouse chorioallantoic branching (2017) Development, 144, pp. 63-73
  • Moussaieff, A., Rouleau, M., Kitsberg, D., Cohen, M., Levy, G., Barasch, D., Nemirovski, A., Amit, M., Glycolysis-mediated changes in acetyl-CoA and histone acetylation control the early differentiation of embryonic stem cells (2015) Cell Metab., 21, pp. 392-402
  • Mullen, A.R., Hu, Z., Shi, X., Jiang, L., Boroughs, L.K., Kovacs, Z., Boriack, R., Linehan, W.M., Oxidation of alpha-ketoglutarate is required for reductive carboxylation in cancer cells with mitochondrial defects (2014) Cell Rep., 7, pp. 1679-1690
  • Nagaraj, R., Sharpley, M.S., Chi, F., Braas, D., Zhou, Y., Kim, R., Clark, A.T., Banerjee, U., Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation (2017) Cell, 168, pp. 210-223. , (e11)
  • Needham, J., Chemical Embryology (1931), University Press Cambridge; Nüsslein-Volhard, C., Wieschaus, E., Mutations affecting segment number and polarity in Drosophila (1980) Nature, 287, pp. 795-801
  • O'connor, R., The metabolism of cell division (1950) Br. J. Exp. Pathol., 31, p. 390
  • O'connor, R., Growth and aerobic glycolysis in the retina of the chicken embryo (1952) Nature, 169, p. 246
  • Oginuma, M., Moncuquet, P., Xiong, F., Karoly, E., Chal, J., Guevorkian, K., Pourquié, O., A gradient of glycolytic activity coordinates FGF and Wnt signaling during elongation of the body axis in amniote embryos (2017) Dev. Cell, 40, pp. 342-353. , (e10)
  • Ou, Q., King-Jones, K., What goes up must come down: transcription factors have their say in making ecdysone pulses (2013) Current topics in Developmental Biology, pp. 35-71. , Elsevier
  • Palsson-McDermott, E.M., O'neill, L.A., The Warburg effect then and now: from cancer to inflammatory diseases (2013) BioEssays, 35, pp. 965-973
  • Panopoulos, A.D., Yanes, O., Ruiz, S., Kida, Y.S., Diep, D., Tautenhahn, R., Herrerías, A., Lutz, M., The metabolome of induced pluripotent stem cells reveals metabolic changes occurring in somatic cell reprogramming (2012) Cell Res., 22, pp. 168-177
  • Parks, S.K., Chiche, J., Pouysségur, J., Disrupting proton dynamics and energy metabolism for cancer therapy (2013) Nat. Rev. Cancer, 13, pp. 611-623
  • Pegoraro, C., Figueiredo, A.L., Maczkowiak, F., Pouponnot, C., Eychène, A., Monsoro-Burq, A.H., PFKFB4 controls embryonic patterning via Akt signalling independently of glycolysis (2015) Nat. Commun., 6, p. 5953
  • Pfeiffer, T., Schuster, S., Bonhoeffer, S., Cooperation and competition in the evolution of ATP-producing pathways (2001) Science, 292, pp. 504-507
  • Qiang, L., Fujita, R., Abeliovich, A., Remodeling neurodegeneration: somatic cell reprogramming-based models of adult neurological disorders (2013) Neuron, 78 (6), pp. 957-969
  • Redel, B.K., Brown, A.N., Spate, L.D., Whitworth, K.M., Green, J.A., Prather, R.S., Glycolysis in preimplantation development is partially controlled by the Warburg effect (2012) Mol. Reprod. Dev., 79, pp. 262-271
  • Ren, F., Wu, H., Lei, Y., Zhang, H., Liu, R., Zhao, Y., Chen, X., Chen, L., Quantitative proteomics identification of phosphoglycerate mutase 1 as a novel therapeutic target in hepatocellular carcinoma (2010) Mol. Cancer, 9, p. 81
  • Rider, M.H., Bertrand, L., Vertommen, D., Michels, P.A., Rousseau, G.G., Louis, H., 6‑phosphofructo‑2‑kinase/fructose‑2, 6‑bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis (2004) Biochem. J., 381, pp. 561-579
  • Rodríguez-Colman, M.J., Schewe, M., Meerlo, M., Stigter, E., Gerrits, J., Pras-Raves, M., Sacchetti, A., Snippert, H.J., Interplay between metabolic identities in the intestinal crypt supports stem cell function (2017) Nature, 543, pp. 424-427
  • Ryall, J.G., Dell'Orso, S., Derfoul, A., Juan, A., Zare, H., Feng, X., Clermont, D., Fulco, M., The NAD+-dependent SIRT1 deacetylase translates a metabolic switch into regulatory epigenetics in skeletal muscle stem cells (2015) Cell Stem Cell, 16, pp. 171-183
  • Schell, J.C., Olson, K.A., Jiang, L., Hawkins, A.J., Van Vranken, J.G., Xie, J., Egnatchik, R.A., Rutter, J., A role for the mitochondrial pyruvate carrier as a repressor of the Warburg effect and colon cancer cell growth (2014) Mol. Cell, 56, pp. 400-413
  • Schuster, S., Boley, D., Möller, P., Stark, H., Kaleta, C., Mathematical models for explaining the Warburg effect: a review focused on ATP and biomass production (2015) Biochem. Soc. Trans., 43, pp. 1187-1194
  • Semenza, G.L., HIF-1: mediator of physiological and pathophysiological responses to hypoxia (2000) J. Appl. Physiol., 88, pp. 1474-1480
  • Shi, Y.G., Tsukada, Y.-I., The discovery of histone demethylases (2013) Cold Spring Harb. Perspect. Biol., 5
  • Shim, H., Dolde, C., Lewis, B.C., Wu, C.-S., Dang, G., Jungmann, R.A., Dalla-Favera, R., Dang, C.V., c-Myc transactivation of LDH-A: implications for tumor metabolism and growth (1997) Proc. Natl. Acad. Sci., 94, pp. 6658-6663
  • Shim, E.-H., Livi, C.B., Rakheja, D., Tan, J., Benson, D., Parekh, V., Kho, E.-Y., Velu, S., L‑2‑Hydroxyglutarate: an epigenetic modifier and putative oncometabolite in renal cancer (2014) Cancer Discov., 4, pp. 1290-1298
  • Suda, T., Takubo, K., Semenza, G.L., Metabolic regulation of hematopoietic stem cells in the hypoxic niche (2011) Cell Stem Cell, 9, pp. 298-310
  • Sullivan, L.B., Gui, D.Y., Hosios, A.M., Bush, L.N., Freinkman, E., Vander Heiden, M.G., Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells (2015) Cell, 162, pp. 552-563
  • Szablewski, L., Expression of glucose transporters in cancers (2013) Biochim. Biophys. Acta Rev. Cancer, 1835, pp. 164-169
  • Tanimura, T., Shepard, T., Glucose metabolism by rat embryos in vitro (1970) Proc. Soc. Exp. Biol. Med., 135, pp. 51-54
  • Teleman, A.A., Metabolism meets development at Wiston House (2016) Development, 143, pp. 3045-3049
  • Tennessen, J.M., Baker, K.D., Lam, G., Evans, J., Thummel, C.S., The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth (2011) Cell Metab., 13, pp. 139-148
  • Tennessen, J.M., Bertagnolli, N.M., Evans, J., Sieber, M.H., Cox, J., Thummel, C.S., Coordinated metabolic transitions during Drosophila embryogenesis and the onset of aerobic glycolysis (2014) Genes Genomes Genetics, 4, pp. 839-850
  • Teperino, R., Schoonjans, K., Auwerx, J., Histone methyl transferases and demethylases; can they link metabolism and transcription? (2010) Cell Metab., 12, pp. 321-327
  • TeSlaa, T., Chaikovsky, A.C., Lipchina, I., Escobar, S.L., Hochedlinger, K., Huang, J., Graeber, T.G., Teitell, M.A., α‑Ketoglutarate accelerates the initial differentiation of primed human pluripotent stem cells (2016) Cell Metab., 24, pp. 485-493
  • Venters, S.J., Hultner, M.L., Ordahl, C.P., Somite cell cycle analysis using somite-staging to measure intrinsic developmental time (2008) Dev. Dyn., 237, pp. 377-392
  • Voet, D., Voet, J.G., Biochemistry (2004), 1, p. 591. , John Wiley & Sons Hoboken; Wang, T., Marquardt, C., Foker, J., Aerobic glycolysis during lymphocyte proliferation (1976) Nature, 261, pp. 702-705
  • Wang, Y.-H., Israelsen, W.J., Lee, D., Vionnie, W., Jeanson, N.T., Clish, C.B., Cantley, L.C., Scadden, D.T., Cell-state-specific metabolic dependency in hematopoiesis and leukemogenesis (2014) Cell, 158, pp. 1309-1323
  • Warburg, O., On the origin of cancer cells (1956) Science, 123, pp. 309-314
  • Ward, P.S., Patel, J., Wise, D.R., Abdel-Wahab, O., Bennett, B.D., Coller, H.A., Cross, J.R., Perl, A.E., The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting α-ketoglutarate to 2‑hydroxyglutarate (2010) Cancer Cell, 17, pp. 225-234
  • Weaver, J.R., Susiarjo, M., Bartolomei, M.S., Imprinting and epigenetic changes in the early embryo (2009) Mamm. Genome, 20, pp. 532-543
  • Weinhouse, S., Millington, R.H., Wenner, C.E., Metabolism of neoplastic tissue (1951) Cancer Res., 11, pp. 845-850
  • Wellen, K.E., Hatzivassiliou, G., Sachdeva, U.M., Bui, T.V., Cross, J.R., Thompson, C.B., ATP-citrate lyase links cellular metabolism to histone acetylation (2009) Science, 324, pp. 1076-1080
  • Wise, D.R., DeBerardinis, R.J., Mancuso, A., Sayed, N., Zhang, X.-Y., Pfeiffer, H.K., Nissim, I., McMahon, S.B., Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction (2008) Proc. Natl. Acad. Sci., 105, pp. 18782-18787
  • Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.-H., Ito, S., Xiao, M.-T., Oncometabolite 2‑hydroxyglutarate is a competitive inhibitor of α‑ketoglutarate-dependent dioxygenases (2011) Cancer Cell, 19, pp. 17-30
  • Zheng, X., Boyer, L., Jin, M., Mertens, J., Kim, Y., Ma, L., Hamm, M., Hunter, T., Metabolic reprogramming during neuronal differentiation from aerobic glycolysis to neuronal oxidative phosphorylation (2016) elife, 5

Citas:

---------- APA ----------
Gándara, L. & Wappner, P. (2018) . Metabo-Devo: A metabolic perspective of development. Mechanisms of Development, 154, 12-23.
http://dx.doi.org/10.1016/j.mod.2018.02.004
---------- CHICAGO ----------
Gándara, L., Wappner, P. "Metabo-Devo: A metabolic perspective of development" . Mechanisms of Development 154 (2018) : 12-23.
http://dx.doi.org/10.1016/j.mod.2018.02.004
---------- MLA ----------
Gándara, L., Wappner, P. "Metabo-Devo: A metabolic perspective of development" . Mechanisms of Development, vol. 154, 2018, pp. 12-23.
http://dx.doi.org/10.1016/j.mod.2018.02.004
---------- VANCOUVER ----------
Gándara, L., Wappner, P. Metabo-Devo: A metabolic perspective of development. Mech. Dev. 2018;154:12-23.
http://dx.doi.org/10.1016/j.mod.2018.02.004