publication . Article . 2018

Suboptimal extracellular pH values alter DNA damage response to induced double‐strand breaks

Massonneau, Julien; Ouellet, Camille; Lucien, Fabrice; Dubois, Claire M.; Tyler, Jessica; Boissonneault, Guylain;
Open Access English
  • Published: 01 Feb 2018 Journal: FEBS Open Bio, volume 8, issue 3, pages 416-425 (eissn: 2211-5463, Copyright policy)
  • Publisher: John Wiley and Sons Inc.
Abstract
Conditions leading to unrepaired DNA double‐stranded breaks are potent inducers of genetic instability. Systemic conditions may lead to fluctuation of hydrogen ions in the cellular microenvironment, and we show that small variations in extracellular pH, termed suboptimal pHe, can decrease the efficiency of DNA repair in the absence of intracellular pH variation. Recovery from bleomycin‐induced DNA double‐stranded breaks in fibroblasts proceeded less efficiently at suboptimal pHe values ranging from 7.2 to 6.9, as shown by the persistence of repair foci, reduction of H4K16 acetylation, and chromosomal instability, while senescence or apoptosis remained undetected...
Subjects
free text keywords: Research Article, Research Articles, DNA double‐stranded breaks, DNA repair, genetic instability, histones, pH
50 references, page 1 of 4

1 Jeggo PA, Pearl LH and Carr AM (2016) DNA repair, genome stability and cancer: a historical perspective. Nat Rev Cancer 16, 35–42.26667849 [PubMed]

2 Morita T, Nagaki T, Fukuda I and Okumura K (1992) Clastogenicity of low pH to various cultured mammalian cells. Mutat Res 268, 297–305.1379335 [PubMed]

3 Morita T (1995) Low pH leads to sister‐chromatid exchanges and chromosomal aberrations, and its clastogenicity is S‐dependent. Mutat Res 334, 301–308.7753094 [PubMed]

4 Kato Y, Ozawa S, Miyamoto C, Maehata Y, Suzuki A, Maeda T and Baba Y (2013) Acidic extracellular microenvironment and cancer. Cancer Cell Int 13, 89.24004445 [OpenAIRE] [PubMed]

5 Yuan J, Narayanan L, Rockwell S and Glazer PM (2000) Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Can Res 60, 4372–4376.

6 McCarty MF and Whitaker J (2010) Manipulating tumor acidification as a cancer treatment strategy. Altern Med Rev 15, 264–272.21155627 [PubMed]

7 Neri D and Supuran CT (2011) Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discovery 10, 767–777.21921921 [OpenAIRE] [PubMed]

8 Kitabchi AE, Umpierrez GE, Miles JM and Fisher JN (2009) Hyperglycemic crises in adult patients with diabetes. Diabetes Care 32, 1335–1343.19564476 [OpenAIRE] [PubMed]

9 Sabatini S and Kurtzman NA (2009) Bicarbonate therapy in severe metabolic acidosis. J Am Soc Nephrol 20, 692–695.18322160 [OpenAIRE] [PubMed]

10 Suki WN and Massry SG (1984) Therapy of Renal Diseases and Related Disorders. Nijhoff, Distributors for the United States and Canada, Kluwer. Boston. Dordrecht; Boston Hingham, MA, USA.

11 Kimmoun A, Novy E, Auchet T, Ducrocq N and Levy B (2015) Hemodynamic consequences of severe lactic acidosis in shock states: from bench to bedside. Crit Care 19, 175.25887061 [OpenAIRE] [PubMed]

12 Saito M, Tsounapi P, Oikawa R, Shimizu S, Honda M, Sejima T, Kinoshita Y and Tomita S (2014) Prostatic ischemia induces ventral prostatic hyperplasia in the SHR; possible mechanism of development of BPH. Sci Rep 4, 3822.24448152 [OpenAIRE] [PubMed]

13 Ricciardolo FL, Gaston B and Hunt J (2004) Acid stress in the pathology of asthma. J Allergy Clin Immunol 113, 610–619.15100663 [OpenAIRE] [PubMed]

14 Huang Y and McNamara JO (2004) Ischemic stroke: “acid otoxicity” is a perpetrator. Cell 118, 665–666.15369664 [PubMed]

15 Chi J‐T (2014) Molecular Genetics of Dysregulated pH Homeostasis. Springer, New York.

50 references, page 1 of 4
Abstract
Conditions leading to unrepaired DNA double‐stranded breaks are potent inducers of genetic instability. Systemic conditions may lead to fluctuation of hydrogen ions in the cellular microenvironment, and we show that small variations in extracellular pH, termed suboptimal pHe, can decrease the efficiency of DNA repair in the absence of intracellular pH variation. Recovery from bleomycin‐induced DNA double‐stranded breaks in fibroblasts proceeded less efficiently at suboptimal pHe values ranging from 7.2 to 6.9, as shown by the persistence of repair foci, reduction of H4K16 acetylation, and chromosomal instability, while senescence or apoptosis remained undetected...
Subjects
free text keywords: Research Article, Research Articles, DNA double‐stranded breaks, DNA repair, genetic instability, histones, pH
50 references, page 1 of 4

1 Jeggo PA, Pearl LH and Carr AM (2016) DNA repair, genome stability and cancer: a historical perspective. Nat Rev Cancer 16, 35–42.26667849 [PubMed]

2 Morita T, Nagaki T, Fukuda I and Okumura K (1992) Clastogenicity of low pH to various cultured mammalian cells. Mutat Res 268, 297–305.1379335 [PubMed]

3 Morita T (1995) Low pH leads to sister‐chromatid exchanges and chromosomal aberrations, and its clastogenicity is S‐dependent. Mutat Res 334, 301–308.7753094 [PubMed]

4 Kato Y, Ozawa S, Miyamoto C, Maehata Y, Suzuki A, Maeda T and Baba Y (2013) Acidic extracellular microenvironment and cancer. Cancer Cell Int 13, 89.24004445 [OpenAIRE] [PubMed]

5 Yuan J, Narayanan L, Rockwell S and Glazer PM (2000) Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Can Res 60, 4372–4376.

6 McCarty MF and Whitaker J (2010) Manipulating tumor acidification as a cancer treatment strategy. Altern Med Rev 15, 264–272.21155627 [PubMed]

7 Neri D and Supuran CT (2011) Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discovery 10, 767–777.21921921 [OpenAIRE] [PubMed]

8 Kitabchi AE, Umpierrez GE, Miles JM and Fisher JN (2009) Hyperglycemic crises in adult patients with diabetes. Diabetes Care 32, 1335–1343.19564476 [OpenAIRE] [PubMed]

9 Sabatini S and Kurtzman NA (2009) Bicarbonate therapy in severe metabolic acidosis. J Am Soc Nephrol 20, 692–695.18322160 [OpenAIRE] [PubMed]

10 Suki WN and Massry SG (1984) Therapy of Renal Diseases and Related Disorders. Nijhoff, Distributors for the United States and Canada, Kluwer. Boston. Dordrecht; Boston Hingham, MA, USA.

11 Kimmoun A, Novy E, Auchet T, Ducrocq N and Levy B (2015) Hemodynamic consequences of severe lactic acidosis in shock states: from bench to bedside. Crit Care 19, 175.25887061 [OpenAIRE] [PubMed]

12 Saito M, Tsounapi P, Oikawa R, Shimizu S, Honda M, Sejima T, Kinoshita Y and Tomita S (2014) Prostatic ischemia induces ventral prostatic hyperplasia in the SHR; possible mechanism of development of BPH. Sci Rep 4, 3822.24448152 [OpenAIRE] [PubMed]

13 Ricciardolo FL, Gaston B and Hunt J (2004) Acid stress in the pathology of asthma. J Allergy Clin Immunol 113, 610–619.15100663 [OpenAIRE] [PubMed]

14 Huang Y and McNamara JO (2004) Ischemic stroke: “acid otoxicity” is a perpetrator. Cell 118, 665–666.15369664 [PubMed]

15 Chi J‐T (2014) Molecular Genetics of Dysregulated pH Homeostasis. Springer, New York.

50 references, page 1 of 4
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