Role for the ATPase inhibitory factor 1 in the environmental carcinogen-induced Warburg phenotype

Role for the ATPase inhibitory factor 1 in the environmental carcinogen-induced Warburg phenotype Most tumors undergo metabolic reprogramming towards glycolysis, the so-called Warburg effect, to support growth and survival. Overexpression of IF1, the physiological inhibitor of the F0F1ATPase, has been related to this phenomenon and appears to be a relevant marker in cancer. Environmental contributions to cancer development are now widely accepted but little is known about the underlying intracellular mechanisms. Among the environmental pollutants humans are commonly exposed to, benzo[a]pyrene (B[a]P), the prototype molecule of polycyclic aromatic hydrocarbons (PAHs), is a well-known human carcinogen. Besides apoptotic signals, B[a]P can also induce survival signals in liver cells, both likely involved in cancer promotion. Our previous works showed that B[a]P elicited a Warburg-like effect, thus favoring cell survival. The present study aimed at further elucidating the molecular mechanisms involved in the B[a]P-induced metabolic reprogramming, by testing the possible involvement of IF1. We presently demonstrate, both in vitro and in vivo, that PAHs, especially B[a]P, strongly increase IF1 expression. Such an increase, which might rely on β2-adrenergic receptor activation, notably participates to the B[a]P-induced glycolytic shift and cell survival in liver cells. By identifying IF1 as a target of PAHs, this study provides new insights about how environmental factors may contribute to related carcinogenesis. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Scientific Reports Springer Journals

Role for the ATPase inhibitory factor 1 in the environmental carcinogen-induced Warburg phenotype

12 pages
Read Article

Loading next page...
 
/lp/springer_journal/role-for-the-atpase-inhibitory-factor-1-in-the-environmental-lB0190cX3Q
Publisher
Nature Publishing Group UK
Copyright
Copyright © 2017 by The Author(s)
Subject
Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
eISSN
2045-2322
D.O.I.
10.1038/s41598-017-00269-7
Publisher site
See Article on Publisher Site

Abstract

Most tumors undergo metabolic reprogramming towards glycolysis, the so-called Warburg effect, to support growth and survival. Overexpression of IF1, the physiological inhibitor of the F0F1ATPase, has been related to this phenomenon and appears to be a relevant marker in cancer. Environmental contributions to cancer development are now widely accepted but little is known about the underlying intracellular mechanisms. Among the environmental pollutants humans are commonly exposed to, benzo[a]pyrene (B[a]P), the prototype molecule of polycyclic aromatic hydrocarbons (PAHs), is a well-known human carcinogen. Besides apoptotic signals, B[a]P can also induce survival signals in liver cells, both likely involved in cancer promotion. Our previous works showed that B[a]P elicited a Warburg-like effect, thus favoring cell survival. The present study aimed at further elucidating the molecular mechanisms involved in the B[a]P-induced metabolic reprogramming, by testing the possible involvement of IF1. We presently demonstrate, both in vitro and in vivo, that PAHs, especially B[a]P, strongly increase IF1 expression. Such an increase, which might rely on β2-adrenergic receptor activation, notably participates to the B[a]P-induced glycolytic shift and cell survival in liver cells. By identifying IF1 as a target of PAHs, this study provides new insights about how environmental factors may contribute to related carcinogenesis.

Journal

Scientific Reports – Springer Journals

Published: Mar 15, 2017

References

  • Mitochondria-mediated energy adaption in cancer: the H(+)-ATP synthase-geared switch of metabolism in human tumors
    Sánchez-Aragó, M; Formentini, L; Cuezva, JM
  • Regulation of mitochondrial ATP synthase in cardiac pathophysiology
    Long, Q; Yang, K; Yang, Q
  • The ATPase Inhibitory Factor 1 (IF1): A master regulator of energy metabolism and of cell survival
    García-Bermúdez, J; Cuezva, JM
  • The ATP synthase is involved in generating mitochondrial cristae morphology
    Paumard, P
  • From ATP to PTP and Back: A Dual Function for the Mitochondrial ATP Synthase
    Bernardi, P; Lisa, F; Fogolari, F; Lippe, G
  • The H(+)-ATP synthase: a gate to ROS-mediated cell death or cell survival
    Martínez-Reyes, I; Cuezva, JM
  • Inhibitory and anchoring domains in the ATPase inhibitor protein IF1 of bovine heart mitochondrial ATP synthase
    Zanotti, F; Raho, G; Gaballo, A; Papa, S
  • Modulation of the oligomerization state of the bovine F1-ATPase inhibitor protein, IF1, by pH
    Cabezon, E; Butler, PJ; Runswick, MJ; Walker, JE
  • Role of cellular energetics in ischemia-reperfusion and ischemic preconditioning of myocardium
    Hassinen, IE; Vuorinen, KH; Ylitalo, K; Ala-Rämi, A
  • IF(1): setting the pace of the F(1)F(o)-ATP synthase
    Campanella, M; Parker, N; Tan, CH; Hall, AM; Duchen, MR
  • The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response
    Formentini, L; Sánchez-Aragó, M; Sánchez-Cenizo, L; Cuezva, JM
  • The IF(1) inhibitor protein of the mitochondrial F(1)F(0)-ATPase
    Green, DW; Grover, GJ
  • Expression, regulation and clinical relevance of the ATPase inhibitory factor 1 in human cancers
    Sánchez-Aragó, M
  • Reciprocal activation between ATPase inhibitory factor 1 and NF-κB drives hepatocellular carcinoma angiogenesis and metastasis
    Song, R
  • Up-regulation of the ATPase inhibitory factor 1 (IF1) of the mitochondrial H+-ATP synthase in human tumors mediates the metabolic shift of cancer cells to a Warburg phenotype
    Sánchez-Cenizo, L
  • IF1 limits the apoptotic-signalling cascade by preventing mitochondrial remodelling
    Faccenda, D; Tan, CH; Seraphim, A; Duchen, MR; Campanella, M
  • Association of carcinogenic polycyclic aromatic hydrocarbon emissions and smoking with lung cancer mortality rates on a global scale
    Motorykin, O; Matzke, MM; Waters, KM; Massey Simonich, SL
  • Carcinogenic activity of benzo[a]pyrene in a 2 year oral study in Wistar rats
    Wester, PW
  • Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures
  • Benzo[a]pyrene-induced nitric oxide production acts as a survival signal targeting mitochondrial membrane potential
    Hardonnière, K
  • The environmental carcinogen benzo[a]pyrene induces a Warburg-like metabolic reprogramming dependent on NHE1 and associated with cell survival
    Hardonnière, K
  • Multiple apoptotic pathways induced by p53-dependent acidification in benzo[a]pyrene-exposed hepatic F258 cells
    Huc, L
  • Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles
    Subramanian, A
  • Gene-expression signature of vascular invasion in hepatocellular carcinoma
    Mínguez, B
  • InSilico DB genomic datasets hub: an efficient starting point for analyzing genome-wide studies in GenePattern, Integrative Genomics Viewer, and R/Bioconductor
    Coletta, A
  • Gas chromatography-tandem mass spectrometry analysis of 52 monohydroxylated metabolites of polycyclic aromatic hydrocarbons in hairs of rats after controlled exposure
    Grova, N; Salquebre, G; Appenzeller, BM
  • Identification of Na+/H+ exchange as a new target for toxic polycyclic aromatic hydrocarbons
    Huc, L
  • Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation
    Podechard, N
  • Aryl hydrocarbon receptor-independent up-regulation of intracellular calcium concentration by environmental polycyclic aromatic hydrocarbons in human endothelial HMEC-1 cells
    Mayati, A; Ferrec, E; Lagadic-Gossmann, D; Fardel, O
  • Apoptotic mitochondrial dysfunction induced by benzo(a)pyrene in liver epithelial cells: role of p53 and pHi changes
    Huc, L
  • Induction of intracellular calcium concentration by environmental benzo(a)pyrene involves a β2-adrenergic receptor/adenylyl cyclase/Epac-1/inositol 1,4,5-trisphosphate pathway in endothelial cells
    Mayati, A
  • Ligand-regulated internalization and recycling of human beta 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors
    Zastrow, M; Kobilka, BK
  • ATPase inhibitory factor 1 is a prognostic marker and contributes to proliferation and invasion of human gastric cancer cells
    Yin, T; Lu, L; Xiong, Z; Wei, S; Cui, D
  • Mitochondrial and postmitochondrial survival signaling in cancer
    Yadav, N; Chandra, D
  • Identification by differential display of the IF1 inhibitor peptide of ATP synthase/ATPase as a gene inducible in rat liver by pregnenolone 16alpha-carbonitrile
    Jiménez, BD; Quattrochi, LC; Yockey, CB; Guzelian, PS
  • Hypoxia-inducible factor 1α regulates the expression of the mitochondrial ATPase inhibitor protein (IF1) in rat liver
    Huang, LJ; Chuang, IC; Dong, HP; Yang, RC
  • β2-adrenergic receptors mediate cardioprotection through crosstalk with mitochondrial cell death pathways
    Fajardo, G
  • The β2-adrenoceptor agonist formoterol stimulates mitochondrial biogenesis
    Wills, LP
  • PKA Phosphorylates the ATPase Inhibitory Factor 1 and Inactivates Its Capacity to Bind and Inhibit the Mitochondrial H+-ATP Synthase
    García-Bermúdez, J
  • Induction of an ATPase inhibitor protein by propylthiouracil and protection against paracetamol (acetaminophen) hepatotoxicity in the rat
    Banerjee, A
  • The oligomycin-sensitivity conferring protein of mitochondrial ATP synthase: emerging new roles in mitochondrial pathophysiology
    Antoniel, M
  • Anesthetic cardioprotection in relation to mitochondria: basic science
    Mio, Y; Uezono, S; Kitahata, H
  • Assessing actual contribution of IF1, inhibitor of mitochondrial FoF1, to ATP homeostasis, cell growth, mitochondrial morphology, and cell viability
    Fujikawa, M; Imamura, H; Nakamura, J; Yoshida, M
  • The inhibitor protein (IF1) of the F1F0-ATPase modulates human osteosarcoma cell bioenergetics
    Barbato, S; Sgarbi, G; Gorini, G; Baracca, A; Solaini, G
  • IF1, the endogenous regulator of the F(1)F(o)-ATPsynthase, defines mitochondrial volume fraction in HeLa cells by regulating autophagy
    Campanella, M; Seraphim, A; Abeti, R; Casswell, E; Echave, P; Duchen, MR
  • The interplay between mitochondrial dynamics and mitophagy
    Twig, G; Shirihai, OS
  • During autophagy mitochondria elongate, are spared from degradation and sustain cell viability
    Gomes, LC; Benedetto, G; Scorrano, L

You’re reading a free preview. Subscribe to read the entire article.

Try 2 weeks free now

DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

or browse the journals available

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off

Sign up
for free
Start 14 day
Free Trial