Intracellular pH regulation by Na+/H+ exchanger-1 (NHE1) is required for growth factor-induced mammary branching morphogenesis

Abramoff, 2004, Image Processing with ImageJ, Biophotonics Int., 11, 36

Andersen, 2011, The metastasis-promoting protein S100A4 regulates mammary branching morphogenesis, Dev. Biol., 352, 181, 10.1016/j.ydbio.2010.12.033

Bianchini, 1997, The p42/p44 mitogen-activated protein kinase cascade is determinant in mediating activation of the Na+/H+ exchanger (NHE1 isoform) in response to growth factors, J. Biol. Chem., 272, 271, 10.1074/jbc.272.1.271

Booth, 2007, Roles of transforming growth factor-alpha in mammary development and disease, Growth Factors, 25, 227, 10.1080/08977190701750698

Bundy, 2005, C/EBPbeta-2 confers EGF-independent growth and disrupts the normal acinar architecture of human mammary epithelial cells, Mol. Cancer, 4, 43, 10.1186/1476-4598-4-43

Busser, 2011, The multiple roles of amphiregulin in human cancer, Biochim. Biophys. Acta, 1816, 119

Bussolino, 1989, Stimulation of the Na+/H+ exchanger in human endothelial cells activated by granulocyte- and granulocyte-macrophage-colony-stimulating factor. Evidence for a role in proliferation and migration, J. Biol. Chem., 264, 18284, 10.1016/S0021-9258(18)51460-5

Cardone, 2005, The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis, Nat. Rev. Cancer, 5, 786, 10.1038/nrc1713

Casey, 2010, Sensors and regulators of intracellular pH, Nat. Rev. Mol. Cell Biol., 11, 50, 10.1038/nrm2820

Chambard, 1986, Intracellular pH controls growth factor-induced ribosomal protein S6 phosphorylation and protein synthesis in the G0–G1 transition of fibroblasts, Exp. Cell Res., 164, 282, 10.1016/0014-4827(86)90029-7

Chiang, 2008, EGF upregulates Na+/H+ exchanger NHE1 by post-translational regulation that is important for cervical cancer cell invasiveness, J. Cell. Physiol., 214, 810, 10.1002/jcp.21277

Counillon, 1993, A point mutation of the Na+/H+ exchanger gene (NHE1) and amplification of the mutated allele confer amiloride resistance upon chronic acidosis, Proc. Natl. Acad. Sci. U. S. A., 90, 4508, 10.1073/pnas.90.10.4508

Delvaux, 1990, Amiloride and analogues inhibit Na(+)-H+ exchange and cell proliferation in AR42J pancreatic cell line, Am. J. Physiol., 259, G842

Denker, 2002, Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1, J. Cell Biol., 159, 1087, 10.1083/jcb.200208050

Dimri, 2005, Mammary epithelial cell transformation: insights from cell culture and mouse models, Breast Cancer Res., 7, 171, 10.1186/bcr1275

Ewald, 2008, Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis, Dev. Cell, 14, 570, 10.1016/j.devcel.2008.03.003

Fata, 2004, Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes, Breast Cancer Res., 6, 1, 10.1186/bcr634

Fata, 2007, The MAPK(ERK-1,2) pathway integrates distinct and antagonistic signals from TGFalpha and FGF7 in morphogenesis of mouse mammary epithelium, Dev. Biol., 306, 193, 10.1016/j.ydbio.2007.03.013

Furukawa, 1999, Epidermal growth factor protects rat epithelial cells against acid-induced damage through the activation of Na+/H+ exchangers, J. Pharmacol. Exp. Ther., 288, 620

Ghishan, 1992, Epidermal growth factor up-regulates intestinal Na+/H+ exchange activity, Proc. Soc. Exp. Biol. Med., 201, 289, 10.3181/00379727-201-43510

Grandin, 1990, Cycling of intracellular pH during cell division of Xenopus embryos is a cytoplasmic activity depending on protein synthesis and phosphorylation, J. Cell Biol., 111, 523, 10.1083/jcb.111.2.523

Grimm, 2006, Keratin 6 is not essential for mammary gland development, Breast Cancer Res., 8, R29, 10.1186/bcr1504

Grinstein, 1989, Na+/H+ exchange and growth factor-induced cytosolic pH changes. Role in cellular proliferation, Biochim. Biophys. Acta, 988, 73, 10.1016/0304-4157(89)90004-X

Gudjonsson, 2005, Myoepithelial cells: their origin and function in breast morphogenesis and neoplasia, J. Mammary Gland Biol. Neoplasia, 10, 261, 10.1007/s10911-005-9586-4

Haimovici, 1994, Different modulation of hepatocellular Na+/H+ exchange activity by insulin and EGF, Am. J. Physiol., 267, G364

Harguindey, 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

Harguindey, 2009, Proton transport inhibitors as potentially selective anticancer drugs, Anticancer Res., 29, 2127

Horvat, 1992, Tumour cell proliferation is abolished by inhibitors of Na+/H+ and HCO3-/Cl- exchange, Eur. J. Cancer, 29A, 132

Hynes, 2010, Mammary gland growth factors: roles in normal development and in cancer, Cold Spring Harb. Perspect. Biol., 2, a003186, 10.1101/cshperspect.a003186

James-Kracke, 1992, Quick and accurate method to convert BCECF fluorescence to pHi: calibration in three different types of cell preparations, J. Cell. Physiol., 151, 596, 10.1002/jcp.1041510320

Jang, 2006, The Na(+)/H(+) exchanger is a major pH regulator in GABAergic presynaptic nerve terminals synapsing onto rat CA3 pyramidal neurons, J. Neurochem., 99, 1224, 10.1111/j.1471-4159.2006.04168.x

Johnstone, 2007, Epidermal growth factor and sphingosine-1-phosphate stimulate Na+/H+ exchanger activity in the human placental syncytiotrophoblast, Am. J. Physiol. Regul. Integr. Comp. Physiol., 293, R2290, 10.1152/ajpregu.00328.2007

Khaled, 2001, Trophic factor withdrawal: p38 mitogen-activated protein kinase activates NHE1, which induces intracellular alkalinization, Mol. Cell. Biol., 21, 7545, 10.1128/MCB.21.22.7545-7557.2001

Khokha, 2010, Mammary gland reprogramming: metalloproteinases couple form with function, Cold Spring Harb. Perspect. Biol., 3

Khurana, 1996, Brush border phosphatidylinositol 3-kinase mediates epidermal growth factor stimulation of intestinal NaCl absorption and Na+/H+ exchange, J. Biol. Chem., 271, 9919, 10.1074/jbc.271.17.9919

Kintner, 2004, Increased tolerance to oxygen and glucose deprivation in astrocytes from Na(+)/H(+) exchanger isoform 1 null mice, Am. J. Physiol. Cell Physiol., 287, C12, 10.1152/ajpcell.00560.2003

Kintner, 2005, Stimulation of astrocyte Na+/H+ exchange activity in response to in vitro ischemia depends in part on activation of ERK1/2, Am. J. Physiol. Cell Physiol., 289, C934, 10.1152/ajpcell.00092.2005

Koliakos, 2008, NHE-1: a molecular target for signalling and cell matrix interactions, Connect. Tissue Res., 49, 157, 10.1080/03008200802151581

Lagadic-Gossmann, 2004, Alterations of intracellular pH homeostasis in apoptosis: origins and roles, Cell Death Differ., 11, 953, 10.1038/sj.cdd.4401466

Li, 2003, Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells, Proc. Natl. Acad. Sci. U. S. A., 100, 15853, 10.1073/pnas.2136825100

Luo, 2007, ERK1/2-p90RSK-mediated phosphorylation of Na+/H+ exchanger isoform 1. A role in ischemic neuronal death, J. Biol. Chem., 282, 28274, 10.1074/jbc.M702373200

Ma, 1994, Activation of Na+/H+ exchange by platelet-derived growth factor involves phosphatidylinositol 3'-kinase and phospholipase C gamma, J. Biol. Chem., 269, 30734, 10.1016/S0021-9258(18)43875-6

Malo, 2007, Mitogen-activated protein kinase-dependent activation of the Na+/H+ exchanger is mediated through phosphorylation of amino acids Ser770 and Ser771, J. Biol. Chem., 282, 6292, 10.1074/jbc.M611073200

Martin, 2011, Intracellular pH gradients in migrating cells, Am. J. Physiol. Cell Physiol., 300, C490, 10.1152/ajpcell.00280.2010

Matthews, 2011, Anti-tumour/metastasis effects of the potassium-sparing diuretic amiloride: An orally active anti-cancer drug waiting for its call-of-duty?, Int. J. Cancer, 129, 2051, 10.1002/ijc.26156

McCubrey, 2007, Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance, Biochim. Biophys. Acta, 1773, 1263, 10.1016/j.bbamcr.2006.10.001

McLean, 2000, Malignant gliomas display altered pH regulation by NHE1 compared with nontransformed astrocytes, Am. J. Physiol. Cell Physiol., 278, C676, 10.1152/ajpcell.2000.278.4.C676

McManus, 2006, The relationship between histone H3 phosphorylation and acetylation throughout the mammalian cell cycle, Biochem. Cell Biol., 84, 640, 10.1139/o06-086

McNally, 2011, Molecular regulators of pubertal mammary gland development, Ann. Med., 43, 212, 10.3109/07853890.2011.554425

Meima, 2009, The sodium-hydrogen exchanger NHE1 is an Akt substrate necessary for actin filament reorganization by growth factors, J. Biol. Chem., 284, 26666, 10.1074/jbc.M109.019448

Moolenaar, 1983, Na+/H+ exchange and cytoplasmic pH in the action of growth factors in human fibroblasts, Nature, 304, 645, 10.1038/304645a0

Moor, 1999, Protein kinase-mediated regulation of the Na(+)/H(+) exchanger in the rat myocardium by mitogen-activated protein kinase-dependent pathways, J. Biol. Chem., 274, 22985, 10.1074/jbc.274.33.22985

Pasic, 2011, Sustained activation of the HER1-ERK1/2-RSK signaling pathway controls myoepithelial cell fate in human mammary tissue, Genes Dev., 25, 1641, 10.1101/gad.2025611

Pedersen, 2006, The Na+/H+ exchanger NHE1 in stress-induced signal transduction: implications for cell proliferation and cell death, Pflugers Arch., 452, 249, 10.1007/s00424-006-0044-y

Pedersen, 2007, Regulation of mitogen-activated protein kinase pathways by the plasma membrane Na+/H+ exchanger, NHE1, Arch. Biochem. Biophys., 462, 195, 10.1016/j.abb.2006.12.001

Putney, 2003, Na-H exchange-dependent increase in intracellular pH times G2/M entry and transition, J. Biol. Chem., 278, 44645, 10.1074/jbc.M308099200

Putney, 2004, Expression profile of genes regulated by activity of the Na-H exchanger NHE1, BMC Genomics, 5, 46, 10.1186/1471-2164-5-46

Putney, 2002, The changing face of the Na+/H+ exchanger, NHE1: structure, regulation, and cellular actions, Annu. Rev. Pharmacol. Toxicol., 42, 527, 10.1146/annurev.pharmtox.42.092001.143801

Quinn, 1996, The role of Na+/H+ exchange and growth factors in pulmonary artery smooth muscle cell proliferation, Am. J. Respir. Cell Mol. Biol., 14, 139, 10.1165/ajrcmb.14.2.8630263

Ren, 2010, ERK1/2-Akt1 crosstalk regulates arteriogenesis in mice and zebrafish, J. Clin. Invest., 120, 1217, 10.1172/JCI39837

Reshkin, 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, 10.1096/fj.00-0029com

Santen, 2002, The role of mitogen-activated protein (MAP) kinase in breast cancer, J. Steroid Biochem. Mol. Biol., 80, 239, 10.1016/S0960-0760(01)00189-3

Schneider, 2009, The Na+/H+ exchanger NHE1 is required for directional migration stimulated via PDGFR-alpha in the primary cilium, J. Cell Biol., 185, 163, 10.1083/jcb.200806019

Schwertfeger, 2009, Fibroblast growth factors in development and cancer: insights from the mammary and prostate glands, Curr. Drug Targets, 10, 632, 10.2174/138945009788680419

Shen, 1979, Intracellular pH and the sodium requirement at fertilisation, Nature, 282, 87, 10.1038/282087a0

Slepkov, 2007, Structural and functional analysis of the Na+/H+ exchanger, Biochem. J., 401, 623, 10.1042/BJ20061062

Smith, 1990, Differential keratin gene expression in developing, differentiating, preneoplastic, and neoplastic mouse mammary epithelium, Cell Growth Differ., 1, 161

Smith, 1995, Transforming growth factor-alpha promotes mammary tumorigenesis through selective survival and growth of secretory epithelial cells, Am. J. Pathol., 147, 1081

Steffan, 2009, Na+/H+ exchangers and RhoA regulate acidic extracellular pH-induced lysosome trafficking in prostate cancer cells, Traffic, 10, 737, 10.1111/j.1600-0854.2009.00904.x

Steffan, 2010, HGF-induced invasion by prostate tumor cells requires anterograde lysosome trafficking and activity of Na+−H+ exchangers, J. Cell Sci., 123, 1151, 10.1242/jcs.063644

Sternlicht, 2008, The ADAM17-amphiregulin-EGFR axis in mammary development and cancer, J. Mammary Gland Biol. Neoplasia, 13, 181, 10.1007/s10911-008-9084-6

Sternlicht, 2005, Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin, Development, 132, 3923, 10.1242/dev.01966

Sternlicht, 2006, Hormonal and local control of mammary branching morphogenesis, Differentiation, 74, 365, 10.1111/j.1432-0436.2006.00105.x

Stock, 2006, Role of the Na/H exchanger NHE1 in cell migration, Acta Physiol (Oxf.), 187, 149, 10.1111/j.1748-1716.2006.01543.x

Stock, 2009, Protons make tumor cells move like clockwork, Pflugers Arch., 458, 981, 10.1007/s00424-009-0677-8

Stock, 2005, Migration of human melanoma cells depends on extracellular pH and Na+/H+ exchange, J. Physiol., 567, 225, 10.1113/jphysiol.2005.088344

Stock, 2008, Protons extruded by NHE1: digestive or glue?, Eur. J. Cell Biol., 87, 591, 10.1016/j.ejcb.2008.01.007

Strazzabosco, 1995, Intracellular pH regulation in Hep G2 cells: effects of epidermal growth factor, transforming growth factor-alpha, and insulinlike growth factor-II on Na+/H+ exchange activity, Hepatology, 22, 588

Stull, 2003, Expression of the IGFs, IGF-IR and IGFBPs in the normal mammary gland and breast, Breast Dis., 17, 15, 10.3233/BD-2003-17103

Stuwe, 2007, pH dependence of melanoma cell migration: protons extruded by NHE1 dominate protons of the bulk solution, J. Physiol., 585, 351, 10.1113/jphysiol.2007.145185

Svegliati-Baroni, 1999, The Na+/H+ exchanger modulates the fibrogenic effect of oxidative stress in rat hepatic stellate cells, J. Hepatol., 30, 868, 10.1016/S0168-8278(99)80141-X

Takahashi, 1999, p90(RSK) is a serum-stimulated Na+/H+ exchanger isoform-1 kinase. Regulatory phosphorylation of serine 703 of Na+/H+ exchanger isoform-1, J. Biol. Chem., 274, 20206, 10.1074/jbc.274.29.20206

Thomas, 1979, Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ, Biochemistry, 18, 2210, 10.1021/bi00578a012

Tominaga, 1998, Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading, Mol. Biol. Cell, 9, 2287, 10.1091/mbc.9.8.2287

Tominaga, 1998, p160ROCK mediates RhoA activation of Na-H exchange, EMBO J., 17, 4712, 10.1093/emboj/17.16.4712

Tsuta, 2011, Using the mitosis-specific marker anti-phosphohistone H3 to assess mitosis in pulmonary neuroendocrine carcinomas, Am. J. Clin. Pathol., 136, 252, 10.1309/AJCPDXFOPXGEF0RP

Turturro, 2004, Troglitazone acts on cellular pH and DNA synthesis through a peroxisome proliferator-activated receptor gamma-independent mechanism in breast cancer-derived cell lines, Clin. Cancer Res., 10, 7022, 10.1158/1078-0432.CCR-04-0879

Van Lookeren Campagne, 1989, Cyclic-AMP-induced elevation of intracellular pH precedes, but does not mediate, the induction of prespore differentiation in Dictyostelium discoideum, Development, 105, 401, 10.1242/dev.105.2.401

von Lintig, 2000, Ras activation in human breast cancer, Breast Cancer Res. Treat., 62, 51, 10.1023/A:1006491619920

Wakabayashi, 2006, Intracellular pH as a determinant of vascular smooth muscle function, J. Vasc. Res., 43, 238, 10.1159/000091235

Wang, 2008, Gene inactivation of Na+/H+ exchanger isoform 1 attenuates apoptosis and mitochondrial damage following transient focal cerebral ischemia, Eur. J. Neurosci., 28, 51, 10.1111/j.1460-9568.2008.06304.x

Webb, 1981, Direct measurement of intracellular pH changes in Xenopus eggs at fertilization and cleavage, J. Cell Biol., 91, 562, 10.1083/jcb.91.2.562

Wickenden, 2010, Key signalling nodes in mammary gland development and cancer. Signalling downstream of PI3 kinase in mammary epithelium: a play in 3 Akts, Breast Cancer Res., 12, 202, 10.1186/bcr2558

Wiseman, 2003, Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis, J. Cell Biol., 162, 1123, 10.1083/jcb.200302090

Woodward, 1998, The role of mammary stroma in modulating the proliferative response to ovarian hormones in the normal mammary gland, J. Mammary Gland Biol. Neoplasia, 3, 117, 10.1023/A:1018738721656

Yan, 2001, The Nck-interacting kinase (NIK) phosphorylates the Na+−H+ exchanger NHE1 and regulates NHE1 activation by platelet-derived growth factor, J. Biol. Chem., 276, 31349, 10.1074/jbc.M102679200

Yang, 2010, Inhibition of Na(+)/H(+) exchanger 1 by 5-(N-ethyl-N-isopropyl) amiloride reduces hypoxia-induced hepatocellular carcinoma invasion and motility, Cancer Lett., 295, 198, 10.1016/j.canlet.2010.03.001

Yang, 2011, Suppression of Na(+)/H (+) exchanger 1 by RNA interference or amiloride inhibits human hepatoma cell line SMMC-7721 cell invasion, Med. Oncol., 28, 385, 10.1007/s12032-010-9447-x