Skip to main content

Advertisement

SpringerLink
Log in

Role of Cell Metabolism and Mitochondrial Function During Adult Neurogenesis

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Brain is the major consumer of glucose in the human body, whose pattern of consumption changes through lifetime, decreasing during adolescence up to adulthood. This evidence leads to the hypothesis that, in cerebral developmental stages, glycolysis might be the driving force for the high-energy requirement. Furthermore, several studies claim that neurogenesis process is accompanied by a shift into mitochondrial oxidative metabolism. Herein, we discuss recent work about cell metabolism during neuronal differentiation process, in particular the mitochondrial role in cellular bioenergy dynamics.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Ramón CS (1928) Degeneration and regeneration of the nervous system. Hafner Publishing Company, New York

    Google Scholar 

  2. Balu DT, Lucki I (2009) Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 33(3):232–252

    Article  PubMed  Google Scholar 

  3. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130(2):391–399

    Article  CAS  PubMed  Google Scholar 

  4. Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z (2009) Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci 29(14):4408–4419

    Article  CAS  PubMed  Google Scholar 

  5. Tropepe V, Craig CG, Morshead CM, van der Kooy D (1997) Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17(20):7850–7859

    CAS  PubMed  Google Scholar 

  6. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24(38):8354–8365

    Article  CAS  PubMed  Google Scholar 

  7. Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36(8):1790–1795

    Article  PubMed  Google Scholar 

  8. Palmer TD, Takahashi J, Gage FH (1997) The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8(6):389–404

    Article  CAS  PubMed  Google Scholar 

  9. Reynolds BA, Weiss S (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175(1):1–13

    Article  CAS  PubMed  Google Scholar 

  10. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255(5052):1707–1710

    Article  CAS  PubMed  Google Scholar 

  11. Raineteau O, Rietschin L, Gradwohl G, Guillemot F, Gähwiler BH (2004) Neurogenesis in hippocampal slice cultures. Mol Cell Neurosci 26(2):241–250

    Article  CAS  PubMed  Google Scholar 

  12. Mistry SK, Keefer EW, Cunningham BA, Edelman GM, Crossin KL (2002) Cultured rat hippocampal neural progenitors generate spontaneously active neural networks. Proc Natl Acad Sci 99(3):1621–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417(6884):39–44

    Article  CAS  PubMed  Google Scholar 

  14. Song H, Stevens CF, Gage FH (2002) Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5(5):438–445

    CAS  PubMed  Google Scholar 

  15. Burns TC, Verfaillie CM, Low WC (2009) Stem cells for ischemic brain injury: a critical review. J Comp Neurol 515(1):125–144

    Article  PubMed  PubMed Central  Google Scholar 

  16. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC et al (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16(23):7599–7609

    CAS  PubMed  Google Scholar 

  17. Markakis EA, Gage FH (1999) Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 406(4):449–460

    Article  CAS  PubMed  Google Scholar 

  18. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415(6875):1030–1034

    Article  PubMed  CAS  Google Scholar 

  19. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410(6826):372–376

    Article  CAS  PubMed  Google Scholar 

  20. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12(5):578–584

    Article  PubMed  PubMed Central  Google Scholar 

  21. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, Eriksson PS (2000) Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20(8):2896–2903

    CAS  PubMed  Google Scholar 

  22. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2(10):894–897

    Article  CAS  PubMed  Google Scholar 

  23. Liu J, Solway K, Messing RO, Sharp FR (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci 18(19):7768–7778

    CAS  PubMed  Google Scholar 

  24. van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1(3):191–198

    Article  PubMed  CAS  Google Scholar 

  25. Panchision DM (2009) The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 220(3):562–568

    Article  CAS  PubMed  Google Scholar 

  26. Simon MC, Keith B (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9(4):285–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Maltepe E, Krampitz GW, Okazaki KM, Red-horse K, Mak W, Simon MC et al (2005) Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 132:3393–3403

    Article  CAS  PubMed  Google Scholar 

  28. Dings J, Meixensberger J, Jager A, Roosen K (1998) Clinical experience with 118 brain tissue oxygen partial pressure catheter probes. Neurosurgery 43(5):1082–1095

    Article  CAS  PubMed  Google Scholar 

  29. Da Silveira Paulsen B, Souza Da Silveira M, Galina A, Kastrup Rehen S (2013) Pluripotent stem cells as a model to study oxygen metabolism in neurogenesis and neurodevelopmental disorders. Arch Biochem Biophys 534(1–2):3–10

    Article  CAS  Google Scholar 

  30. Pourié G, Blaise S, Trabalon M, Nédélec E, Guéant J-L, Daval J-L (2006) Mild, non-lesioning transient hypoxia in the newborn rat induces delayed brain neurogenesis associated with improved memory scores. Neuroscience 140(4):1369–1379

    Article  PubMed  CAS  Google Scholar 

  31. Chen C-T, Hsu S-H, Wei Y-H (2012) Mitochondrial bioenergetic function and metabolic plasticity in stem cell differentiation and cellular reprogramming. Biochim Biophys Acta 1820(5):571–576

    Article  CAS  PubMed  Google Scholar 

  32. Vieira HLA, Alves PM, Vercelli A (2011) Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog Neurobiol 93(3):444–455

    Article  CAS  PubMed  Google Scholar 

  33. Dirnagl U, Meisel A (2008) Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning? Neuropharmacology 55(3):334–344

    Article  CAS  PubMed  Google Scholar 

  34. Naylor M, Bowen KK, Sailor K a, Dempsey RJ, Vemuganti R (2005) Preconditioning-induced ischemic tolerance stimulates growth factor expression and neurogenesis in adult rat hippocampus. Neurochem Int 47(8):565–572

    Article  CAS  PubMed  Google Scholar 

  35. Ara J, De montpellier S (2013) Hypoxic-preconditioning enhances the regenerative capacity of neural stem/progenitors in subventricular zone of newborn piglet brain. Stem Cell Res 11(2):669–686

    Article  CAS  PubMed  Google Scholar 

  36. Varela-Nallar L, Rojas-Abalos M, Abbott AC, Moya EA, Iturriaga R, Inestrosa NC (2014) Chronic hypoxia induces the activation of the Wnt/beta-catenin signaling pathway and stimulates hippocampal neurogenesis in wild-type and APPswe-PS1DeltaE9 transgenic mice in vivo. Front Cell Neurosci 8:17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Zhang K, Zhou Y, Zhao T, Wu L, Huang X, Wu K et al (2015) Reduced cerebral oxygen content in the DG and SVZ in situ promotes neurogenesis in the adult rat brain in vivo. PLoS One 10(10)

  38. Pedroso D, Nunes AR, Diogo LN, Oudot C, Monteiro EC, Brenner C, Vieira HL (2016) Hippocampal neurogenesis response: what can we expect from two different models of hypertension? Brain Res 1646:199–206

    Article  CAS  PubMed  Google Scholar 

  39. Prozorovski T, Schneider R, Berndt C, Hartung H-P, Aktas O (2015) Redox-regulated fate of neural stem progenitor cells. Biochim Biophys Acta 1850(8):1543–1554

    Article  CAS  PubMed  Google Scholar 

  40. Ostrakhovitch EA, Semenikhin OA (2013) The role of redox environment in neurogenic development. Arch Biochem Biophys 534(1–2):44–54

    Article  CAS  PubMed  Google Scholar 

  41. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD et al (2011) Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8(1):59–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Almeida AS, Soares NL, Vieira M, Gramsbergen JB, Vieira HLA (2016) Carbon monoxide releasing molecule-A1 (CORM-A1) improves neurogenesis: increase of neuronal differentiation yield by preventing cell death. PLoS One 11(5):e0154781

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Tsatmali M, Walcott EC, Crossin KL (2005) Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors. Brain Res 1040(1–2):137–150

    Article  CAS  PubMed  Google Scholar 

  44. Cho YM, Kwon S, Pak Y, Seol H, Choi Y, Park D et al (2006) Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 348:1472–1478

    Article  CAS  PubMed  Google Scholar 

  45. Nitti M, Furfaro AL, Cevasco C, Traverso N, Marinari UM, Pronzato MA et al (2010) PKC delta and NADPH oxidase in retinoic acid-induced neuroblastoma cell differentiation. Cell Signal 22(5):828–835

    Article  CAS  PubMed  Google Scholar 

  46. Suzukawa K, Miura K, Mitsushita J, Resau J, Hirose K, Crystal R et al (2000) Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J Biol Chem 275(18):13175–13178

    Article  CAS  PubMed  Google Scholar 

  47. Schmidt-Kastner R, van Os J, Steinbusch H WM, Schmitz C (2006) Gene regulation by hypoxia and the neurodevelopmental origin of schizophrenia. Schizophr Res 84(2–3):253–271

    Article  PubMed  Google Scholar 

  48. Le Belle JE, Orozco NM, Paucar A a, Saxe JP, Mottahedeh J, Pyle AD et al (2011) Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8(1):59–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kennedy K a M, Sandiford SDE, Skerjanc IS, Li SS-C (2012) Reactive oxygen species and the neuronal fate. Cell Mol Life Sci 69(2):215–221

    Article  PubMed  CAS  Google Scholar 

  50. Margineantu DH, Hockenbery DM (2016) Mitochondrial functions in stem cells. Curr Opin Genet Dev 38:110–117

    Article  CAS  PubMed  Google Scholar 

  51. Lavelle A (1963) Mitochondrial changes in developing neurons. Am J Anat 113:175–187

    Article  CAS  PubMed  Google Scholar 

  52. Andrew W, Johnson H (1956) Staining mitochondria in fixed blood smears. Stain Technol 31(1):21–23

    Article  CAS  PubMed  Google Scholar 

  53. Kasahara A, Scorrano L (2014) Mitochondria: from cell death executioners to regulators of cell differentiation. Trends Cell Biol 24(12):761–770

    Article  CAS  PubMed  Google Scholar 

  54. Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St. John JC (2007) Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 120(22):4025–4034

    Article  CAS  PubMed  Google Scholar 

  55. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CA, Ramalho-Santos J et al (2011) Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS One 6(6):e20914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhang J, Khvorostov I, Hong JS, Oktay Y, Vergnes L, Nuebel E et al (2011) UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 30(24):4860–4873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chen C-TCT, Hsu S-H, Wei Y-HYH (2009) Upregulation of mitochondrial function and antioxidant defense in the differentiation of stem cells. Biochim Biophys Acta 1800(3):1–7

    Google Scholar 

  58. Vayssiere JL, Larcher JC, Gros F, Croizat B (1987) Changes in the beta-subunit of mitochondrial F1 ATPase during neurogenesis. Biochem Biophys Res Commun 145(1):443–452

    Article  CAS  PubMed  Google Scholar 

  59. Cordeau-Lossouarn L, Vayssiere JL, Larcher JC, Gros F, Croizat B (1991) Mitochondrial maturation during neuronal differentiation in vivo and in vitro. Biol Cell 71(1–2):57–65

    Article  CAS  PubMed  Google Scholar 

  60. Zheng X, Boyer L, Jin M, Mertens J, Kim Y, Ma L et al (2016) Metabolic reprogramming during neuronal differentiation from aerobic glycolysis to neuronal oxidative phosphorylation. Elife 5:e13374

    PubMed  PubMed Central  Google Scholar 

  61. O’Brien LC, Keeney PM, Bennett JPJ (2015) Differentiation of human neural stem cells into motor neurons stimulates mitochondrial biogenesis and decreases glycolytic flux. Stem Cells Dev 24(17):1984–1994

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Agostini M, Romeo F, Inoue S, Niklison-Chirou MV, Elia AJ, Dinsdale D et al (2016) Metabolic reprogramming during neuronal differentiation. Cell Death Differ 23(9):1502–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Cheng A, Wan R, Yang J, Kamimura N, Son T, Ouyang X et al (2012) Involvement of PGC-1α in the formation and maintenance of neuronal dendritic spines. Nat Commun 3:1250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Pereira SL, Grãos M, Rodrigues AS, Anjo SI, Carvalho R a, Oliveira PJ et al (2013) Inhibition of mitochondrial complex III blocks neuronal differentiation and maintains embryonic stem cell pluripotency. PLoS One 8(12):e82095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Schneider L, Giordano S, Zelickson BR, S Johnson M, A Benavides G, Ouyang X et al (2011) Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radic Biol Med 51(11):2007–2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A (2007) Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med 4(Suppl 1):S60–S67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. St John JC, Ramalho-Santos J, Gray HL, Petrosko P, Rawe VY, Navara CS et al (2005) The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7(3):141–153

    Article  CAS  PubMed  Google Scholar 

  68. Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U (2011) Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 29(3):486–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Han YH, Kim SH, Kim SZ, Park WH (2008) Antimycin A as a mitochondria damage agent induces an S phase arrest of the cell cycle in HeLa cells. Life Sci 83(9–10):346–355

    Article  CAS  PubMed  Google Scholar 

  70. Han YH, Kim SH, Kim SZ, Park WH (2008) Antimycin A as a mitochondrial electron transport inhibitor prevents the growth of human lung cancer A549 cells. Oncol Rep 20(3):689–693

    CAS  PubMed  Google Scholar 

  71. Han YH, Park WH (2009) Growth inhibition in antimycin A treated-lung cancer Calu-6 cells via inducing a G1 phase arrest and apoptosis. Lung Cancer 65(2):150–160

    Article  PubMed  Google Scholar 

  72. Stoll E, Makin R, Sweet I, Trevelyan A, Miwa S, Horner P et al (2015) Neural stem cells in the adult subventricular zone oxidize fatty acids to produce energy and support neurogenic activity. Stem Cells 33(7):2306–2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Wilkins HM, Harris JL, Carl SM, Lezi E, Lu J, Selfridge JE et al (2014) Oxaloacetate activates brain mitochondrial biogenesis, enhances the insulin pathway, reduces inflammation and stimulates neurogenesis. Hum Mol Genet 23(24):6528–6541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Mils V, Bosch S, Roy J, Bel-Vialar S, Belenguer P, Pituello F et al (2015) Mitochondrial reshaping accompanies neural differentiation in the developing spinal cord. PLoS One 10(5):e0128130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Wilkerson DC, Sankar U (2011) Mitochondria: a sulfhydryl oxidase and fission GTPase connect mitochondrial dynamics with pluripotency in embryonic stem cells. Int J Biochem Cell Biol 43(9):1252–1256

    Article  CAS  PubMed  Google Scholar 

  76. Fathi A, Hatami M, Vakilian H, Han C-L, Chen Y-J, Baharvand H et al (2014) Quantitative proteomics analysis highlights the role of redox hemostasis and energy metabolism in human embryonic stem cell differentiation to neural cells. J Proteom 101:1–16

    Article  CAS  Google Scholar 

  77. Komarova SV, Ataullakhanov FI, Globus RK (2000) Bioenergetics and mitochondrial transmembrane potential during differentiation of cultured osteoblasts. Am J Physiol Cell Physiol 279(4):C1220–C1229

    CAS  PubMed  Google Scholar 

  78. Kim J-M, Jeong D, Kang HK, Jung SY, Kang SS, Min B-M (2007) Osteoclast precursors display dynamic metabolic shifts toward accelerated glucose metabolism at an early stage of RANKL-stimulated osteoclast differentiation. Cell Physiol Biochem 20(6):935–946

    Article  CAS  PubMed  Google Scholar 

  79. Pattappa G, Heywood HK, de Bruijn JD, Lee DA (2011) The metabolism of human mesenchymal stem cells during proliferation and differentiation. J Cell Physiol 226(10):2562–2570

    Article  CAS  PubMed  Google Scholar 

  80. Mischen BT, Follmar KE, Moyer KE, Buehrer B, Olbrich KC, Levin LS et al (2008) Metabolic and functional characterization of human adipose-derived stem cells in tissue engineering. Plast Reconstr Surg 122(3):725–738

    Article  CAS  PubMed  Google Scholar 

  81. Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT (2006) Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol 290(4):C1139–C1146

    Article  CAS  PubMed  Google Scholar 

  82. Grayson WL, Zhao F, Bunnell B, Ma T (2007) Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358(3):948–953

    Article  CAS  PubMed  Google Scholar 

  83. Miharada K, Karlsson G, Rehn M, Rörby E, Siva K, Cammenga J et al (2011) Cripto regulates hematopoietic stem cells as a hypoxic-niche-related factor through cell surface receptor GRP78. Cell Stem Cell 9(4):330–344

    Article  CAS  PubMed  Google Scholar 

  84. Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Ahmed I, Olson EN et al (2010) The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7(3):380–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Unwin RD, Smith DL, Blinco D, Wilson CL, Miller CJ, Evans CA et al (2006) Quantitative proteomics reveals posttranslational control as a regulatory factor in primary hematopoietic stem cells. Blood 107(12):4687–4695

    Article  CAS  PubMed  Google Scholar 

  86. Alvarez Z, Hyrossova P, Perales JC, Alcantara S (2014) Neuronal progenitor maintenance requires lactate metabolism and PEPCK-M-directed cataplerosis. Cereb Cortex 26(3):1046–1058

    Article  PubMed  Google Scholar 

  87. Bond AM, Ming G-L, Song H (2015) Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell 17(4):385–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Homem CCF, Steinmann V, Burkard TR, Jais A, Esterbauer H, Knoblich JA (2014) Ecdysone and mediator change energy metabolism to terminate proliferation in Drosophila neural stem cells. Cell 158(4):874–888

    Article  CAS  PubMed  Google Scholar 

  89. Jády AG, Nagy ÁM, Kőhidi T, Ferenczi S, Tretter L, Madarász E (2016) Differentiation-dependent energy production and metabolite utilization: a comparative study on neural stem cells, neurons, and astrocytes. Stem Cells Dev 25(13):scd.2015.0388

    Article  CAS  Google Scholar 

  90. Gascon S, Murenu E, Masserdotti G, Ortega F, Russo GL, Petrik D et al (2016) Identification and successful negotiation of a metabolic checkpoint in direct neuronal reprogramming. Cell Stem Cell 18(3):396–409

    Article  CAS  PubMed  Google Scholar 

  91. Almeida AS, Sonnewald U, Alves PM, Vieira HLA (2016) Carbon monoxide improves neuronal differentiation and yield by increasing the functioning and number of mitochondria. J Neurochem 138(3):423–435

    Article  CAS  PubMed  Google Scholar 

  92. Fornazari M, Nascimento IC, Nery A a, da Silva CCC, Kowaltowski AJ, Ulrich H (2011) Neuronal differentiation involves a shift from glucose oxidation to fermentation. J Bioenerg Biomembr 43(5):531–539

    Article  CAS  PubMed  Google Scholar 

  93. Aubert A, Costalat R, Magistretti PJ, Pellerin L (2005) Brain lactate kinetics: modeling evidence for neuronal lactate uptake upon activation. Proc Natl Acad Sci 102(45):16448–16453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Pellerin L, Bouzier-Sore A-K, Aubert A, Serres S, Merle M, Costalat R et al (2007) Activity-dependent regulation of energy metabolism by astrocytes: an uptade. Glia 55:1251–1262

    Article  PubMed  Google Scholar 

  95. Pellerin L, Magistretti PJ (2012) Sweet sixteen for ANLS. J Cereb Blood Flow 32(7):1152–1166

    Article  CAS  Google Scholar 

  96. Wohnsland S, Burgers HF, Kuschinsky W, Maurer MH (2010) Neurons and neuronal stem cells survive in glucose-free lactate and in high glucose cell culture medium during normoxia and anoxia. Neurochem Res 35(10):1635–1642

    Article  CAS  PubMed  Google Scholar 

  97. Uittenbogaard M, Baxter KK, Chiaramello A (2010) The neurogenic basic helix-loop-helix transcription factor NeuroD6 confers tolerance to oxidative stress by triggering an antioxidant response and sustaining the mitochondrial biomass. ASN Neuro 2(2):115–133

    Article  CAS  Google Scholar 

  98. Zhao F, Wu T, Lau A, Jiang T, Huang Z, Wang X-J et al (2009) Nrf2 promotes neuronal cell differentiation. Free Radic Biol Med 47(6):867–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Dringen R, Hoepken HH, Minich T, Ruedig C (2007) Handbook of neurochemistry and molecular neurobiology: brain energetics. In: Gibson GE, Dienel GA, Lajtha A (eds) Integration of molecular and cellular processes. Springer US, Boston, pp 41–62

    Google Scholar 

  100. Zhao Y, Pan X, Zhao J, Wang Y, Peng Y, Zhong C (2009) Decreased transketolase activity contributes to impaired hippocampal neurogenesis induced by thiamine deficiency. J Neurochem 111(2):537–546

    Article  CAS  PubMed  Google Scholar 

  101. Kathagen A, Schulte A, Balcke G, Phillips HS, Martens T, Matschke J et al (2013) Hypoxia and oxygenation induce a metabolic switch between pentose phosphate pathway and glycolysis in glioma stem-like cells. Acta Neuropathol 126(5):763–780

    Article  CAS  PubMed  Google Scholar 

  102. Dekkers MPJ, Barde Y-A (2013) Developmental biology. Programmed cell death in neuronal development. Science 340(6128):39–41

    Article  CAS  PubMed  Google Scholar 

  103. Boya P, De La Rosa EJ (2005) Cell death in early neural life. Birth Defects Res Part C Embryo Today Rev 75(4):281–293

    Article  CAS  Google Scholar 

  104. Wang S, Rosengren LE, Hamberger A, Haglid KG (1998) An acquired sensitivity to H2O2-induced apoptosis during neuronal differentiation of NT2/D1 cells. Neuroreport 9(14):3207–3211

    Article  CAS  PubMed  Google Scholar 

  105. de la Rosa EJ, de Pablo F (2000) Cell death in early neural development: beyond the neurotrophic theory. Trends Neurosci 23(10):454–458

    Article  PubMed  Google Scholar 

  106. Yeo W, Gautier J (2004) Early neural cell death: dying to become neurons. Dev Biol 274(2):233–244

    Article  CAS  PubMed  Google Scholar 

  107. Buss R, Oppenheim R (2004) Special review based on a presentation made at the 16th international congress of the IFAA role of programmed cell death in normal neuronal development and function. Anat Sci Int 79:191–197

    Article  PubMed  Google Scholar 

  108. Galluzzi L, Kepp O, Kroemer G (2012) Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 13(12):780–788

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The funding was provided by Fundação para a Ciência e a Tecnologia (Grant Nos. ANR/NEU-NMC/0022/2012, IF/00185/2012, SFRH/BD/78440/2011).

Author information

Authors and Affiliations

  1. CEDOC, NOVA Medical School/Faculdade de Ciência Médicas, Universidade Nova de Lisboa, Campo dos Mártires da Pátria 130, 1169-056, Lisboa, Portugal

    Ana S. Almeida & Helena L. A. Vieira

  2. Instituto de Tecnologia Química e Biológica (ITQB), Universidade Nova de Lisboa, Apartado 127, 2781-901, Oeiras, Portugal

    Ana S. Almeida

  3. Instituto de Biologia Experimental e Tecnológica (iBET), Apartado 12, 2781-901, Oeiras, Portugal

    Ana S. Almeida & Helena L. A. Vieira

Authors
  1. Ana S. Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Helena L. A. Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helena L. A. Vieira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Almeida, A.S., Vieira, H.L.A. Role of Cell Metabolism and Mitochondrial Function During Adult Neurogenesis. Neurochem Res 42, 1787–1794 (2017). https://doi.org/10.1007/s11064-016-2150-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-016-2150-3

Keywords

Search

Navigation