Role of pHi, and proton transporters in oncogene-driven neoplastic transformation

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1638, 2014, Pages

  Reshkin, Stephan Joel ^a   Greco, Maria Raffaella ^a   Cardone, Rosa Angela ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Angiogenesis; Growth factors; Invasion; NHE1; pH and cancer; Tumour microenvironment

Indexed keywords

ABNORMALITY; ALKALINIZATION; BIOCHEMISTRY; CANCER; CARCINOGEN; CATION; CYTOLOGY; DEVELOPMENTAL BIOLOGY; FUNCTIONAL ROLE; GENE EXPRESSION; HYDROGEN; OXYGEN; PATHOLOGY; PH; PHYSIOLOGY; TRANSFORMATION; TUMOR;

CATION TRANSPORT PROTEIN; PROTON PUMP; SLC9A1 PROTEIN, HUMAN; SODIUM PROTON EXCHANGE PROTEIN;

ANGIOGENESIS; BIOLOGICAL MODEL; CELL TRANSFORMATION; CHEMISTRY; CYTOPLASM; GENETICS; GROWTH FACTORS; HUMAN; INVASION; METABOLISM; NHE1; ONCOGENE; PH; PH AND CANCER; PHYSIOLOGY; REVIEW; TUMOR MICROENVIRONMENT;

ANGIOGENESIS; GROWTH FACTORS; INVASION; NHE1; PH AND CANCER; TUMOUR MICROENVIRONMENT;

CATION TRANSPORT PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; CYTOPLASM; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; ONCOGENES; PROTON PUMPS; SODIUM-HYDROGEN ANTIPORTER;

EID: 84893498721     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0100     Document Type: Review

References (86)

1. Harguindey S, Arranz JL, Wahl ML, Orive G, Reshkin SJ. 2009 Proton transport inhibitors as potentially selective anticancer drugs. Anticancer Res. 29, 2127-2136.
2. + antiporter in the etiopathogenesis and treatment of cancer: two faces of the same coin-one single nature. Biochim. Biophys. Acta 1756, 1-24.
3. Provost JJ, Wallert MA. 2013 Inside out: targeting NHE1 as an intracellular and extracellular regulator of cancer progression. Chem. Biol. Drug Des. 81, 85-101. (doi:10.1111/cbdd.12035)
4. + exchanger in metastasis. Nat. Rev. Cancer 5, 786-795. (doi:10.1038/nrc1713)
5. Hashim AI, Zhang X, Wojtkowiak JW, Martinez GV, Gillies RJ. 2011 Imaging pH and metastasis. NMR Biomed. 24, 582-591.
6. Calderon-Montano J, Burgos-Moron E, Perez-Guerrero C, Salvador J, Robles A, Lopez-Lazaro M. 2011 Role of the Intracellular pH in the metabolic switch between oxidative phosphorylation and aerobic glycolysis: relevance to cancer. WebmedCentral CANCER 2, WMC001716.
7. Porporato PE, Dhup S, Dadhich RK, Copetti T, Sonveaux P. 2011 Anticancer targets in the glycolytic metabolism of tumors: a comprehensive review. Front. Pharmacol. 2, 49.
8. Boedtkjer E, Bunch L, Pedersen SF. 2012 Physiology, pharmacology and pathophysiology of the pH regulatory transport proteins NHE1 and NBCn1: similarities, differences, and implications for cancer therapy. Curr. Pharm. Des. 18, 1345-1371. (doi:10.2174/138161212799504830)
9. Parks SK, Chiche J, Pouyssegur J. 2011 pH control mechanisms of tumor survival and growth. J. Cell Physiol. 226, 299-308. (doi:10.1002/jcp.22400)
10. Doppler W, Jaggi R, Groner B. 1987 Induction of v-mos and activated Ha-ras oncogene expression in quiescent NIH 3T3 cells causes intracellular alkalinisation and cell-cycle progression. Gene 54, 147-153. (doi:10.1016/0378-1119(87)90357-X)
11. Hagag N, Lacal JC, Graber M, Aaronson S, Viola MV. 1987 Microinjection of ras p21 induces a rapid rise in intracellular pH. Mol. Cell Biol. 7, 1984-1988.
12. + exchangerdependent 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. (doi:10.1096/fj.00-0029com)
13. Hanahan D, Weinberg RA. 2011 Hallmarks of cancer: the next generation. Cell 144, 646-674. (doi:10.1016/j.cell.2011.02.013)
14. Warburg O. 1956 On respiratory impairment in cancer cells. Science 124, 269-270.
15. Kuwata F, Suzuki N, Otsuka K, Taguchi M, Sasai Y, Wakino H, Ito M, Ebihara S, Suzuki K. 1991 Enzymatic regulation of glycolysis and gluconeogenesis in rabbit periodontal ligament under various physiological pH conditions. J. Nihon Univ. Sch. Dent. 33, 81-90. (doi:10.2334/josnusd1959.33.81)
16. Peak M, Al-Habori M, Agius L. 1992 Regulation of glycogen synthesis and glycolysis by insulin, pH and cell volume: interactions between swelling and alkalinization in mediating the effects of insulin. Biochem. J. 282, 797-805.
17. Dietl K et al. 2010 Lactic acid and acidification inhibit TNF secretion and glycolysis of human monocytes. J. Immunol. 184, 1200-1209. (doi:10.4049/jimmunol.0902584)
18. Chiche J, Brahimi-Horn MC, Pouyssegur J. 2010 Tumour hypoxia induces a metabolic shift causing acidosis: a common feature in cancer. J. Cell Mol. Med. 14, 771-794. (doi:10.1111/j.1582-4934.2009.00994.x)
19. Santo-Domingo J, Demaurex N. 2012 Perspectives on: SGP symposium on mitochondrial physiology and medicine: the renaissance of mitochondrial pH. J. Gen. Physiol. 139, 415-423. (doi:10.1085/jgp. 201110767)
20. Webb BA, Chimenti M, Jacobson MP, Barber DL. 2011 Dysregulated pH: a perfect storm for cancer progression. Nat. Rev. Cancer 11, 671-677. (doi:10.1038/nrc3110)
21. Schönichen A, Webb BA, Jacobson MP, Barber DL. 2013 Considering protonation as a posttranslational modification regulating protein structure and function. Annu. Rev. Biophys. 42, 289-314. (doi:10.1146/annurev-biophys-050511-102349)
22. + exchanger precedes apoptotic events in the MNK45 and MNK74 gastric cancer cell lines treated with 2-aminophenoxazine-3-one. Oncol. Rep. 25, 341-346.
23. Chen JL et al. 2010 Lactic acidosis triggers starvation response with paradoxical induction of TXNIP through MondoA. PLoS Genet. 6, e1001093. (doi:10.1371/journal.pgen.1001093)
24. Putney LK, Barber DL. 2004 Expression profile of genes regulated by activity of the Na-H exchanger NHE1. BMC Genomics 5, 46. (doi:10.1186/1471-2164-5-46)
25. Singh RK, Tsan R, Radinsky R. 1997 Influence of the host microenvironment on the clonal selection of human colon carcinoma cells during primary tumor growth and metastasis. Clin. Exp. Metastasis 15, 140-150. (doi:10.1023/A:1018400826845)
26. Reynolds TY, Rockwell S, Glazer PM. 1996 Genetic instability induced by the tumor microenvironment. Cancer Res. 56, 5754-5757.
27. Radinsky R. 1995 Modulation of tumor cell gene expression and phenotype by the organ-specific metastatic environment. Cancer Metastasis Rev. 14, 323-338. (doi:10.1007/BF00690601)
28. Lane N, Martin WF. 2012 The origin of membrane bioenergetics. Cell 151, 1406-1416. (doi:10.1016/j. cell.2012.11.050)
29. Vaupel P, Okunieff P, Neuringer LJ. 1989 Blood flow, tissue oxygenation, pH distribution, and energy metabolism of murine mammary adenocarcinomas during growth. Adv. Exp. Med. Biol. 248, 835-845. (doi:10.1007/978-1-4684-5643-1_95)
30. Griffiths JR. 1991 Are cancer cells acidic? Br. J. Cancer 64, 425-427. (doi:10.1038/bjc. 1991.326)
31. Chiche J, Ilc K, Laferriere J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, Pouyssegur J. 2009 Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 69, 358-368. (doi:10.1158/0008-5472.CAN-08-2470)
32. Supuran CT. 2008 Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov. 7, 168-181. (doi:10.1038/nrd2467)
33. Chiche J, Le Fur Y, Vilmen C, Frassineti F, Daniel L, Halestrap AP, Cozzone PJ, Pouysségur J, Lutz NW. 2012 In vivo pH in metabolic-defective Rastransformed fibroblast tumors: key role of the monocarboxylate transporter, MCT4, for inducing an alkaline intracellular pH. Int. J. Cancer 130, 1511-1520. (doi:10.1002/ijc.26125)
34. Pouyssegur J, Dayan F, Mazure NM. 2006 Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441, 437-443. (doi:10.1038/nature04871)
35. Chiang AC, Massague J. 2008 Molecular basis of metastasis. N. Engl. J. Med. 359, 2814-2823. (doi:10.1056/NEJMra0805239)
36. + exchanger 1 and its clinicopathologic significance in hepatocellular carcinoma. Med. Oncol. 27, 1109-1113. (doi:10.1007/s12032-009-9343-4)
37. McLean LA, Roscoe J, Jorgensen NK, Gorin FA, Cala PM. 2000 Malignant gliomas display altered pH regulation by NHE1 compared with nontransformed astrocytes. Am. J. Physiol. Cell Physiol. 278, C676-C688.
38. + efflux in caveolae. Oncogene 30, 2070-2076. (doi:10.1038/onc.2010.574)
39. Schlappack OK, Zimmermann A, Hill RP. 1991 Glucose starvation and acidosis: effect on experimental metastatic potential, DNA content and MTX resistance of murine tumour cells. Br. J. Cancer 64, 663-670. (doi:10.1038/bjc.1991.378)
40. Rofstad EK. 2000 Microenvironment-induced cancer metastasis. Int. J. Radiat. Biol. 76, 589-605. (doi:10.1080/095530000138259)
41. Moellering RE, Black KC, Krishnamurty C, Baggett BK, Stafford P, Rain M, Gatenby RA, Gillies RJ. 2008 Acid treatment of melanoma cells selects for invasive phenotypes. Clin. Exp. Metastasis 25, 411-425. (doi:10.1007/s10585-008-9145-7)
42. Martinez-Zaguilan R, Seftor EA, Seftor REB, Chu YW, Gillies RJ, Hendrix MJC. 1996 Acidic pH enhances the invasive behavior of human melanoma cells. Clin. Exp. Metastasis 14, 176-186. (doi:10.1007/BF00121214)
43. Giusti I, D'Ascenzo S, Millimaggi D, Taraboletti G, Carta G, Franceschini N, Pavan A, Dolo V. 2008 Cathepsin B mediates the pH-dependent proinvasive activity of tumor-shed microvesicles. Neoplasia 10, 481-488.
44. Rofstad EK, Mathiesen B, Kindem K, Galappathi K. 2006 Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res. 66, 6699-6707. (doi:10.1158/0008-5472.CAN-06-0983)
45. Martin NK, Gaffney EA, Gatenby RA, Maini PK. 2010 Tumour-stromal interactions in acid-mediated invasion: a mathematical model. J. Theor. Biol. 267, 461-470. (doi:10.1016/j.jtbi.2010.08.028)
46. + exchange, motility, and invasion induced by serum deprivation. J. Biol. Chem. 275, 5361-5369. (doi:10.1074/jbc.275.8.5361)
47. Cardone RA et al. 2007 The NHERF1 PDZ2 domain regulates PKA-RhoA-p38-mediated NHE1 activation and invasion in breast tumor cells. Mol. Biol. Cell 18, 1768-1780. (doi:10.1091/mbc.E06-07-0617)
48. Busco G et al. 2010 NHE1 promotes invadopodial ECM proteolysis through acidification of the periinvadopodial space. FASEB J. 24, 3903-3915. (doi:10.1096/fj.09-149518)
49. + exchanger in renal microvillus membrane vesicles. Nature 299, 161-163. (doi:10.1038/299161a0)
50. Cardone RA et al. 2008 HPV16 E7-dependent transformation activates NHE1 through a PKA-RhoAinduced inhibition of p38alpha. PLoS ONE 3, e3529. (doi:10.1371/journal.pone.0003529)
51. + antiporter. Cell 56, 271-280. (doi:10.1016/0092-8674(89)90901-X)
52. Meima ME, Webb BA, Witkowska HE, Barber DL. 2009 The sodium-hydrogen exchanger NHE1 is an Akt substrate necessary for actin filament reorganization by growth factors. J. Biol. Chem. 284, 26 666-26 675. (doi:10.1074/jbc.M109.019448)
53. +) exchanger NHE1 as plasma membrane scaffold in the assembly of signaling complexes. Am. J. Physiol. Cell Physiol. 287, C844-C850. (doi:10.1152/ajpcell.00094.2004)
54. Meima ME, Mackley JR, Barber DL. 2007 Beyond ion translocation: structural functions of the sodium-hydrogen exchanger isoform-1. Curr. Opin. Nephrol. Hypertens. 16, 365-372. (doi:10.1097/MNH.0b013e3281bd888d)
55. + exchanger (NHE1) in breast cancer metastasis. Cancer Res. 73, 1259-1264. (doi:10.1158/0008-5472.CAN-12-4031)
56. + exchanger isoform 1 a potential therapeutic target in cancer? Curr. Med. Chem. 19, 647-660. (doi:10.2174/0929867 12798992101)
57. + exchanger. J. Biol. Chem. 286, 13 096-13 105. (doi:10.1074/jbc.M110.165134)
58. + exchanger, NHE1: structure, regulation, and cellular actions. Annu. Rev. Pharmacol. Toxicol. 42, 527-552. (doi:10.1146/annurev.pharmtox.42.092001.143801)
59. + exchange in pulmonary arterial smooth muscle cells. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L867-L874. (doi:10.1152/ajplung. 00455.2004)
60. + exchanger 1 by 5-(N-ethyl-Nisopropyl) amiloride reduces hypoxia-induced hepatocellular carcinoma invasion and motility. Cancer Lett. 295, 198-204. (doi:10.1016/j.canlet. 2010.03.001)
61. Lucien F, Brochu-Gaudreau K, Arsenault D, Harper K, Dubois CM. 2011 Hypoxia-induced invadopodia formation involves activation of NHE-1 by the p90 ribosomal S6 kinase (p90RSK). PLoS ONE 6, e28851. (doi:10.1371/journal.pone.0028851)
62. Pinheiro C, Longatto-Filho A, Azevedo-Silva J, Casal M, Schmitt FC, Baltazar F. 2012 Role of monocarboxylate transporters in human cancers: state of the art. J. Bioenerg. Biomembr. 44, 127-139. (doi:10.1007/s10863-012-9428-1)
63. +-linked monocarboxylate transporter (MCT1/SLC16A1): a potential therapeutic target for highrisk neuroblastoma. Mol. Pharmacol. 70, 2108-2115. (doi:10.1124/mol.106.026245)
64. Sonveaux P et al. 2008 Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J. Clin. Invest. 118, 3930-3942.
65. Wahl ML, Owen JA, Burd R, Herlands RA, Nogami SS, Rodeck U, Berd D, Leeper DB, Owen CS. 2002 Regulation of intracellular pH in human melanoma: potential therapeutic implications. Mol. Cancer Ther. 1, 617-628.
66. Birsoy K et al. 2013 MCT1-mediated transport of a toxic molecule is an effective strategy for targeting glycolytic tumors. Nat. Genet. 45, 104-108. (doi:10.1038/ng.2471)
67. 3 2 formula buffer in the regulation of intracellular pH of three-dimensional tumor growths. J. Biol. Chem. 286, 13 815-13 826. (doi:10.1074/jbc.M111.219899)
68. Grillon E, Farion R, Fablet K, De Waard M, Tse CM, Donowitz M, Rémy C, Coles JA. 2011 The spatial organization of proton and lactate transport in a rat brain tumor. PLoS ONE 6, e17416. (doi:10.1371/journal.pone.0017416)
69. McDonald PC, Winum JY, Supuran CT, Dedhar S. 2012 Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 3, 84-97.
70. Li X, Liu Y, Alvarez BV, Casey JR, Fliegel L. 2006 A novel carbonic anhydrase II binding site regulates NHE1 activity. Biochemistry 45, 2414-2424. (doi:10.1021/bi051132d)
71. + exchanger. J. Biol. Chem. 277, 36 085-36 091. (doi:10.1074/jbc. M111952200)
72. Goldfeder A. 1953 Some recent developments in the cancer field. J. Am. Med. Womens Assoc. 8, 124-130.
73. + exchanger in rat renal cortical tubules. Am. J. Physiol. 273, C1064-C1074.
74. Matthews H, Ranson M, Kelso MJ. 2011 Antitumour/metastasis effects of the potassium-sparing diuretic amiloride: an orally active anti-cancer drug waiting for its call-of-duty? Int. J. Cancer 129, 2051-2061. (doi:10.1002/ijc.26156)
75. + exchanger. Eur. J. Med. Chem. 38, 547-554. (doi:10.1016/S0223-5234(03)00100-4)
76. Scholz W, Albus U, Counillon L, Gögelein H, Lang HJ, Linz W, Weichert A, Schölkens BA. 1995 Protective effects of HOE642, a selective sodium-hydrogen exchange subtype 1 inhibitor, on cardiac ischaemia and reperfusion. Cardiovasc. Res. 29, 260-268.
77. + antiporter inhibitors. J. Med. Chem. 40, 2017-2034. (doi:10.1021/jm960768n)
78. + exchanger activity is increased in doxorubicin-resistant human colon cancer cells and its modulation modifies the sensitivity of the cells to doxorubicin. Int. J. Cancer 115, 924-929. (doi:10.1002/ijc.20959)
79. i regulation and chemotherapy resistance. Exp. Cell Res. 316, 2538-2553. (doi:10.1016/j.yexcr.2010.06.005)
80. Guzman-Perez A et al. 2001 Discovery of zoniporide: a potent and selective sodium-hydrogen exchanger type 1 (NHE-1) inhibitor with high aqueous solubility. Bioorg. Med. Chem. Lett. 11, 803-807. (doi:10.1016/S0960-894X(01)00059-2)
81. + exchange inhibitor, on ischemia/reperfusion injury. Eur. J. Pharmacol. 404, 221-229. (doi:10.1016/S0014-2999(00)00613-0)
82. + exchanger inhibitors: synthesis and pharmacology of 5-tetrahydroquinolinylidene aminoguanidine derivatives. J. Med. Chem. 45, 3009-3021. (doi:10.1021/jm0104567)
83. + exchanger: a target for therapeutic intervention in cerebral ischemia. In New strategies in stroke intervention. Ionic transporters, pumps, and new channels (ed. A Lucio), pp. 113-128. Totowa, NJ: Humana Press.
84. Loo SY, Chang MK, Chua CS, Kumar AP, Pervaiz S, Clement MV. 2012 NHE-1: a promising target for novel anti-cancer therapeutics. Curr. Pharm. Des. 18, 1372-1382. (doi:10.2174/138161212799504885)
85. + exchanger, pH regulation and cancer. Recent Pat. Anticancer Drug Discov. 8, 85-99.
86. Mengxiao Y, Zhou C, Liu J, Hankins JD, Zheng J. 2011 Luminescent gold nanoparticles with pHdependent membrane adsorption. J. Am. Chem. Soc. 133, 11 014-11 017. (doi:10.1021/ja201930p)