Upregulation of NHE1 protein expression enables glioblastoma cells to escape TMZ-mediated toxicity via increased H+ extrusion, cell migration and survival

Carcinogenesis

Volumn 35, Issue 9, 2014, Pages 2014-2024

  Cong, Damin ^a,b   Zhu, Wen ^b   Shi, Yejie ^b   Pointer, Kelli B ^c   Clark, Paul A ^c   Shen, Hongmei ^d   Kuo, John S ^c,e   Hu, Shaoshan ^a   Sun, Dandan ^a,b,f  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^e UNIVERSITY OF WISCONSIN   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID-BASE EQUILIBRIUM; ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; ASTROCYTES; BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; NEURAL STEM CELLS; SODIUM-HYDROGEN ANTIPORTER; UP-REGULATION;

EID: 84906834191     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgu089     Document Type: Article

References (50)

1. Denysenko,T. et al. (2010) Glioblastoma cancer stem cells: heterogeneity, microenvironment and related therapeutic strategies. Cell Biochem. Funct., 28, 343-351.
2. Dirks,P.B. (2010) Brain tumor stem cells: the cancer stem cell hypothesis writ large. Mol. Oncol., 4, 420-430.
3. Stupp,R. et al.; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups; National Cancer Institute of Canada Clinical Trials Group. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med., 352, 987-996.
4. Harguindey,S. et al. (2005) The role of pH dynamics and the Na+/H+ antiporter in the etiopathogenesis and treatment of cancer. Two faces of the same coin-one single nature. Biochim. Biophys. Acta, 1756, 1-24.
5. Gillies,R.J. et al. (2002) MRI of the tumor microenvironment. J. Magn. Reson. Imaging, 16, 430-450.
6. McLean,L.A. et al. (2000) Malignant gliomas display altered pH regulation by NHE1 compared with nontransformed astrocytes. Am. J. Physiol. Cell Physiol., 278, C676-C688.
7. Cardone,R.A. et al. (2005) The role of disturbed pH dynamics and the Na+/ H+ exchanger in metastasis. Nat. Rev. Cancer, 5, 786-795.
8. Heddleston,J.M. et al. (2012) Hypoxia-induced mixed-lineage leukemia 1 regulates glioma stem cell tumorigenic potential. Cell Death Differ., 19, 428-439.
9. Glunde,K. et al. (2002) Na(+)/H(+) exchange subtype 1 inhibition during extracellular acidification and hypoxia in glioma cells. J. Neurochem., 80, 36-44.
10. Reshkin,S.J. et al. (2000) Na+/H+ exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J., 14, 2185-2197.
11. Lauritzen,G. et al. (2012) The Na+/H+ exchanger NHE1, but not the Na+, HCO3(-) cotransporter NBCn1, regulates motility of MCF7 breast cancer cells expressing constitutively active ErbB2. Cancer Lett., 317, 172-183.
12. Clark,P.A. et al. (2012) Activation of multiple ERBB family receptors mediates glioblastoma cancer stem-like cell resistance to EGFR-targeted inhibition. Neoplasia, 14, 420-428.
13. Zorniak,M. et al. (2012) Differential expression of 2',3'-cyclic-nucleotide 3'-phosphodiesterase and neural lineage markers correlate with glioblastoma xenograft infiltration and patient survival. Clin. Cancer Res., 18, 3628-3636.
14. Svendsen,C.N. et al. (1998) A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods, 85, 141-152.
15. Zhu,W. et al. (2014) WNK1-OSR1 kinase-mediated phospho-activation of Na+-K+-2Cl- cotransporter facilitates glioma migration. Mol. Cancer, 13, 31.
16. Shi,Y. et al. (2013) Stimulation of na(+)/h(+) exchanger isoform 1 promotes microglial migration. PLoS One, 8, e74201.
17. Boyarsky,G. et al. (1993) Intracellular pH regulation in single cultured astrocytes from rat forebrain. Glia, 8, 241-248.
18. Algharabil,J. et al. (2012) Inhibition of Na(+)-K(+)-2Cl(-) cotransporter isoform 1 accelerates temozolomide-mediated apoptosis in glioblastoma cancer cells. Cell. Physiol. Biochem., 30, 33-48.
19. Karki,P. et al. (2011) B-Raf associates with and activates the NHE1 isoform of the Na+/H+ exchanger. J. Biol. Chem., 286, 13096-13105.
20. Lagana,A. et al. (2000) Regulation of the formation of tumor cell pseudopodia by the Na(+)/H(+) exchanger NHE1. J. Cell Sci., 113, 3649-3662.
21. Chanana,V. et al. (2012). The Na+/H+ exchanger-1 as a new molecular target in stroke interventions. In Balestrino,D.M. (ed) Advances in the Preclinical Study of Ischemic Stroke. InTech, Rijeka, Croatia, pp. 497-510.
22. O'Donnell,B.R. et al. (1994) Influence of pH on calcium influx during hypoxia in rat cortical brain slices. Stroke., 25, 171-177.
23. Rochon,P. et al. (2007) Evaluation of BCECF fluorescence ratio imaging to properly measure gastric intramucosal pH variations in vivo. J. Biomed. Opt., 12, 064014.
24. Shahidullah,M. et al. (2009) Responses of sodium-hydrogen exchange to nitric oxide in porcine cultured nonpigmented ciliary epithelium. Invest. Ophthalmol. Vis. Sci., 50, 5851-5858.
25. Altamirano,J. et al. (1998) Regulatory volume decrease and intracellular Ca2+ in murine neuroblastoma cells studied with fluorescent probes. J. Gen. Physiol., 112, 145-160.
26. Könnecke,H. et al. (2013) The role of microglia and matrix metalloproteinases involvement in neuroinflammation and gliomas. Clin. Dev. Immunol., 2013, 914104.
27. Adada,M. et al. (2013) Sphingolipid regulation of ezrin, radixin, and moesin proteins family: implications for cell dynamics. Biochim. Biophys. Acta, 13, 1-11.
28. Harley,W. et al. (2010) Dual inhibition of sodium-mediated proton and calcium efflux triggers non-apoptotic cell death in malignant gliomas. Brain Res., 1363, 159-169.
29. Friedman,H.S. et al. (2000) Temozolomide and treatment of malignant glioma. Clin. Cancer Res., 6, 2585-2597.
30. Maeno,E. et al. (2006) Dysfunction of regulatory volume increase is a key component of apoptosis. FEBS Lett., 580, 6513-6517.
31. Park,J.H. et al. (2012) Fibronectin stimulates migration through lipid raft dependent NHE-1 activation in mouse embryonic stem cells: involvement of RhoA, Ca(2+)/CaM, and ERK. Biochim. Biophys. Acta, 1820, 1618-1627.
32. Wu,K.L. et al. (2004) The NHE1 Na+/H+ exchanger recruits ezrin/radixin/ moesin proteins to regulate Akt-dependent cell survival. J. Biol. Chem., 279, 26280-26286.
33. Paradiso,A. et al. (2004) The Na+-H+ exchanger-1 induces cytoskeletal changes involving reciprocal RhoA and Rac1 signaling, resulting in motility and invasion in MDA-MB-435 cells. Breast Cancer Res., 6, R616-R628.
34. Schneider,L. et al. (2009) The Na+/H+ exchanger NHE1 is required for directional migration stimulated via PDGFR-alpha in the primary cilium. J. Cell Biol., 185, 163-176.
35. Jin,W.N. et al. (2011) [Inhibition of NHE1 promotes hypoxia-induced differentiation of K562 leukemic cells]. Zhongguo Shi Yan Xue Ye Xue Za Zhi, 19, 661-665.
36. López-Lázaro,M. (2008) The warburg effect: why and how do cancer cells activate glycolysis in the presence of oxygen? Anticancer. Agents Med. Chem., 8, 305-312.
37. Loo,S.Y. et al. (2012) NHE-1: a promising target for novel anti-cancer therapeutics. Curr. Pharm. Des., 18, 1372-1382.
38. Putney,L.K. et al. (2002) The changing face of the Na+/H+ exchanger, NHE1: structure, regulation, and cellular actions. Annu. Rev. Pharmacol. Toxicol., 42, 527-552.
39. Reshkin,S.J. et al. (2013) Na+-H+ exchanger, pH regulation and cancer. Recent Pat. Anticancer. Drug Discov., 8, 85-99.
40. Lagadic-Gossmann,D. et al. (2004) Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death Differ., 11, 953-961.
41. Thangaraju,M. et al. (1999) Regulation of acidification and apoptosis by SHP-1 and Bcl-2. J. Biol. Chem., 274, 29549-29557.
42. Thangaraju,M. et al. (1999) Interdependent regulation of intracellular acidification and SHP-1 in apoptosis. Cancer Res., 59, 1649-1654.
43. McHardy,L.M. et al. (2004) The tumor invasion inhibitor dihydromotuporamine C activates RHO, remodels stress fibers and focal adhesions, and stimulates sodium-proton exchange. Cancer Res., 64, 1468-1474.
44. Lin,Y. et al. (2011) NHE1 mediates migration and invasion of HeLa cells via regulating the expression and localization of MT1-MMP. Cell Biochem. Funct., 30, 41-46.
45. Komatsu,K. et al. (2004) Expression and quantitative analysis of matrix metalloproteinase- 2 and -9 in human gliomas. Brain Tumor Pathol., 21, 105-112.
46. Lin,Y. et al. (2011) NHE1 mediates MDA-MB-231 cells invasion through the regulation of MT1-MMP. Exp. Cell Res., 317, 2031-2040.
47. Coccaro,E. et al. (2009) Phenylephrine and sustained acidosis activate the neonatal rat cardiomyocyte Na+/H+ exchanger through phosphorylation of amino acids Ser770 and Ser771. Am. J. Physiol. Heart Circ. Physiol., 297, H846-H858.
48. Roy,S.K. et al. (2010) Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J. Mol. Signal., 5, 10.
49. Matsuyama,S. et al. (2000) Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat. Cell Biol., 2, 318-325.
50. Nakamura,K. et al. (2007) Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient. Eur. J. Neurosci., 26, 3054-3067.