Cancer Cell International | |
Acidic extracellular microenvironment and cancer | |
Yuh Baba2  Toyonobu Maeda3  Atsuko Suzuki3  Yojiro Maehata1  Chihiro Miyamoto1  Shigeyuki Ozawa4  Yasumasa Kato3  | |
[1] Department of Oral Science, Kanagawa Dental University Graduate School of Dentistry, Yokosuka, Japan;Department of General Clinical Medicine, Ohu University School of Dentistry, Koriyama, Japan;Department of Oral Function and Molecular Biology, Ohu University School of Dentistry, 963-8611, Koriyama, Japan;Department of Oral Maxillofacial Surgery, Kanagawa Dental University Graduate School of Dentistry, Yokosuka, Japan | |
关键词: Malignant phenotype; Cancer; Acidic microenvironment; | |
Others : 792931 DOI : 10.1186/1475-2867-13-89 |
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received in 2013-07-25, accepted in 2013-08-29, 发布年份 2013 | |
【 摘 要 】
Acidic extracellular pH is a major feature of tumor tissue, extracellular acidification being primarily considered to be due to lactate secretion from anaerobic glycolysis. Clinicopathological evidence shows that transporters and pumps contribute to H+ secretion, such as the Na+/H+ exchanger, the H+-lactate co-transporter, monocarboxylate transporters, and the proton pump (H+-ATPase); these may also be associated with tumor metastasis. An acidic extracellular pH not only activates secreted lysosomal enzymes that have an optimal pH in the acidic range, but induces the expression of certain genes of pro-metastatic factors through an intracellular signaling cascade that is different from hypoxia. In addition to lactate, CO2 from the pentose phosphate pathway is an alternative source of acidity, showing that hypoxia and extracellular acidity are, while being independent from each other, deeply associated with the cellular microenvironment. In this article, the importance of an acidic extracellular pH as a microenvironmental factor participating in tumor progression is reviewed.
【 授权许可】
2013 Kato et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Warburg O, Posener K, Negelein E: Über den Stoffwechsel der Tumoren (On metabolism of tumors). Biochem Z 1924, 152:319-344.
- [2]Chesler M, Nicholson C: Regulation of intracellular pH in vertebrate central neurons. Brain Res 1985, 325(1–2):313-316.
- [3]Nishisho T, Hata K, Nakanishi M, Morita Y, Sun-Wada GH, Wada Y, Yasui N, Yoneda T: The a3 isoform vacuolar type H+-ATPase promotes distant metastasis in the mouse B16 melanoma cells. Mol Cancer Res 2011, 9(7):845-855.
- [4]Helmlinger G, Sckell A, Dellian M, Forbes NS, Jain RK: Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism. Clin Cancer Res 2002, 8(4):1284-1291.
- [5]Rofstad EK, Mathiesen B, Kindem K, Galappathi K: Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res 2006, 66(13):6699-6707.
- [6]Brizel DM, Schroeder T, Scher RL, Walenta S, Clough RW, Dewhirst MW, Mueller-Klieser W: Elevated tumor lactate concentrations predict for an increased risk of metastases in head-and-neck cancer. Int J Radiat Oncol Biol Phys 2001, 51(2):349-353.
- [7]Walenta S, Chau TV, Schroeder T, Lehr HA, Kunz-Schughart LA, Fuerst A, Mueller-Klieser W: Metabolic classification of human rectal adenocarcinomas: a novel guideline for clinical oncologists? J Cancer Res Clin Oncol 2003, 129(6):321-326.
- [8]Walenta S, Salameh A, Lyng H, Evensen JF, Mitze M, Rofstad EK, Mueller-Klieser W: Correlation of high lactate levels in head and neck tumors with incidence of metastasis. Am J Pathol 1997, 150(2):409-415.
- [9]McFate T, Mohyeldin A, Lu H, Thakar J, Henriques J, Halim ND, Wu H, Schell MJ, Tsang TM, Teahan O, et al.: Pyruvate dehydrogenase complex activity controls metabolic and malignant phenotype in cancer cells. J Biol Chem 2008, 283(33):22700-22708.
- [10]Fischer K, Hoffmann P, Voelkl S, Meidenbauer N, Ammer J, Edinger M, Gottfried E, Schwarz S, Rothe G, Hoves S, et al.: Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 2007, 109(9):3812-3819.
- [11]Yabu M, Shime H, Hara H, Saito T, Matsumoto M, Seya T, Akazawa T, Inoue N: IL-23-dependent and -independent enhancement pathways of IL-17A production by lactic acid. Int Immunol 2011, 23(1):29-41.
- [12]Gottfried E, Kunz-Schughart LA, Ebner S, Mueller-Klieser W, Hoves S, Andreesen R, Mackensen A, Kreutz M: Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood 2006, 107(5):2013-2021.
- [13]Goetze K, Walenta S, Ksiazkiewicz M, Kunz-Schughart LA, Mueller-Klieser W: Lactate enhances motility of tumor cells and inhibits monocyte migration and cytokine release. Int J Oncol 2011, 39(2):453-463.
- [14]Vegran F, Boidot R, Michiels C, Sonveaux P, Feron O: Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kappaB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 2011, 71(7):2550-2560.
- [15]Hunt TK, Aslam RS, Beckert S, Wagner S, Ghani QP, Hussain MZ, Roy S, Sen CK: Aerobically derived lactate stimulates revascularization and tissue repair via redox mechanisms. Antioxid Redox Signal 2007, 9(8):1115-1124.
- [16]Sattler UG, Meyer SS, Quennet V, Hoerner C, Knoerzer H, Fabian C, Yaromina A, Zips D, Walenta S, Baumann M, et al.: Glycolytic metabolism and tumour response to fractionated irradiation. Radiother Oncol 2010, 94(1):102-109.
- [17]Sonveaux P, Copetti T, De Saedeleer CJ, Vegran F, Verrax J, Kennedy KM, Moon EJ, Dhup S, Danhier P, Frerart F, et al.: Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. PLoS One 2012, 7(3):e33418.
- [18]Kim JH, Kim SH, Alfieri AA, Young CW: Quercetin, an inhibitor of lactate transport and a hyperthermic sensitizer of HeLa cells. Cancer Res 1984, 44(1):102-106.
- [19]Hatanaka M, Hanafusa H: Analysis of a functional change in membrane in the process of cell transformation by Rous sarcoma virus; alteration in the characteristics of sugar transport. Virology 1970, 41(4):647-652.
- [20]Kallinowski F, Vaupel P: Concurrent measurements of O2 partial pressures and pH values in human mammary carcinoma xenotransplants. Adv Exp Med Biol 1986, 200:609-621.
- [21]Martin GR, Jain RK: Noninvasive measurement of interstitial pH profiles in normal and neoplastic tissue using fluorescence ratio imaging microscopy. Cancer Res 1994, 54(21):5670-5674.
- [22]Helmlinger G, Yuan F, Dellian M, Jain RK: Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 1997, 3(2):177-182.
- [23]Kayser G, Kassem A, Sienel W, Schulte-Uentrop L, Mattern D, Aumann K, Stickeler E, Werner M, Passlick B, Zur Hausen A: Lactate-dehydrogenase 5 is overexpressed in non-small cell lung cancer and correlates with the expression of the transketolase-like protein 1. Diagn Pathol 2010, 5:22. BioMed Central Full Text
- [24]Koukourakis MI, Giatromanolaki A, Sivridis E, Bougioukas G, Didilis V, Gatter KC, Harris AL: Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis. Br J Cancer 2003, 89(5):877-885.
- [25]Koukourakis MI, Giatromanolaki A, Simopoulos C, Polychronidis A, Sivridis E: Lactate dehydrogenase 5 (LDH5) relates to up-regulated hypoxia inducible factor pathway and metastasis in colorectal cancer. Clin Exp Metastasis 2005, 22(1):25-30.
- [26]Koukourakis MI, Giatromanolaki A, Sivridis E, Gatter KC, Harris AL: Lactate dehydrogenase 5 expression in operable colorectal cancer: strong association with survival and activated vascular endothelial growth factor pathway–a report of the Tumour Angiogenesis Research Group. J Clin Oncol 2006, 24(26):4301-4308.
- [27]Koukourakis MI, Giatromanolaki A, Sivridis E, Gatter KC, Trarbach T, Folprecht G, Shi MM, Lebwohl D, Jalava T, Laurent D, et al.: Prognostic and predictive role of lactate dehydrogenase 5 expression in colorectal cancer patients treated with PTK787/ZK 222584 (vatalanib) antiangiogenic therapy. Clin Cancer Res 2011, 17(14):4892-4900.
- [28]Baron R, Neff L, Louvard D, Courtoy PJ: Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 1985, 101(6):2210-2222.
- [29]Lehenkari P, Hentunen TA, Laitala-Leinonen T, Tuukkanen J, Vaananen HK: Carbonic anhydrase II plays a major role in osteoclast differentiation and bone resorption by effecting the steady state intracellular pH and Ca2+. Exp Cell Res 1998, 242(1):128-137.
- [30]Mobasheri A, Golding S, Pagakis SN, Corkey K, Pocock AE, Fermor B, O’Brien MJ, Wilkins RJ, Ellory JC, Francis MJ: Expression of cation exchanger NHE and anion exchanger AE isoforms in primary human bone-derived osteoblasts. Cell Biol Int 1998, 22(7–8):551-562.
- [31]Biskobing DM, Fan D: Acid pH increases carbonic anhydrase II and calcitonin receptor mRNA expression in mature osteoclasts. Calcif Tissue Int 2000, 67(2):178-183.
- [32]Häbler C: Über den K- und Ca-Gehalt von eiter und Exsudaten und seine Beziehungen zum Entzündungsschmerz. Klin Wochenschrift 1929, 8:1569-1572.
- [33]Dellian M, Helmlinger G, Yuan F, Jain RK: Fluorescence ratio imaging of interstitial pH in solid tumours: effect of glucose on spatial and temporal gradients. Br J Cancer 1996, 74(8):1206-1215.
- [34]Rocha-Gonzalez HI, Herrejon-Abreu EB, Lopez-Santillan FJ, Garcia-Lopez BE, Murbartian J, Granados-Soto V: Acid increases inflammatory pain in rats: Effect of local peripheral ASICs inhibitors. Eur J Pharmacol 2009, 603(1–3):56-61.
- [35]Steen KH, Issberner U, Reeh PW: Pain due to experimental acidosis in human skin: evidence for non-adapting nociceptor excitation. Neurosci Lett 1995, 199(1):29-32.
- [36]Nagae M, Hiraga T, Yoneda T: Acidic microenvironment created by osteoclasts causes bone pain associated with tumor colonization. J Bone Miner Metab 2007, 25(2):99-104.
- [37]Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM, Seuwen K: Proton-sensing G-protein-coupled receptors. Nature 2003, 425(6953):93-98.
- [38]Tomura H, Wang JQ, Liu JP, Komachi M, Damirin A, Mogi C, Tobo M, Nochi H, Tamoto K, Im DS, et al.: Cyclooxygenase-2 expression and prostaglandin E2 production in response to acidic pH through OGR1 in a human osteoblastic cell line. J Bone Miner Res 2008, 23(7):1129-1139.
- [39]Kobayashi Y, Mizoguchi T, Take I, Kurihara S, Udagawa N, Takahashi N: Prostaglandin E2 enhances osteoclastic differentiation of precursor cells through protein kinase A-dependent phosphorylation of TAK1. J Biol Chem 2005, 280(12):11395-11403.
- [40]Iwai K, Koike M, Ohshima S, Miyatake K, Uchiyama Y, Saeki Y, Ishii M: RGS18 acts as a negative regulator of osteoclastogenesis by modulating the acid-sensing OGR1/NFAT signaling pathway. J Bone Miner Res 2007, 22(10):1612-1620.
- [41]Ihara Y, Kihara Y, Hamano F, Yanagida K, Morishita Y, Kunita A, Yamori T, Fukayama M, Aburatani H, Shimizu T, et al.: The G protein-coupled receptor T-cell death-associated gene 8 (TDAG8) facilitates tumor development by serving as an extracellular pH sensor. Proc Natl Acad Sci U S A 2010, 107(40):17309-17314.
- [42]He XD, Tobo M, Mogi C, Nakakura T, Komachi M, Murata N, Takano M, Tomura H, Sato K, Okajima F: Involvement of proton-sensing receptor TDAG8 in the anti-inflammatory actions of dexamethasone in peritoneal macrophages. Biochem Biophys Res Commun 2011, 415(4):627-631.
- [43]Nagae M, Hiraga T, Wakabayashi H, Wang L, Iwata K, Yoneda T: Osteoclasts play a part in pain due to the inflammation adjacent to bone. Bone 2006, 39(5):1107-1115.
- [44]Jasti J, Furukawa H, Gonzales EB, Gouaux E: Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007, 449(7160):316-323.
- [45]Marples MJ: The ecology of human skin. Springfield, IL: Charles C. Thomas; 1965.
- [46]Behne MJ, Barry NP, Hanson KM, Aronchik I, Clegg RW, Gratton E, Feingold K, Holleran WM, Elias PM, Mauro TM: Neonatal development of the stratum corneum pH gradient: localization and mechanisms leading to emergence of optimal barrier function. J Invest Dermatol 2003, 120(6):998-1006.
- [47]Ilic D, Mao-Qiang M, Crumrine D, Dolganov G, Larocque N, Xu P, Demerjian M, Brown BE, Lim ST, Ossovskaya V, et al.: Focal adhesion kinase controls pH-dependent epidermal barrier homeostasis by regulating actin-directed Na+/H+ exchanger 1 plasma membrane localization. Am J Pathol 2007, 170(6):2055-2067.
- [48]Adamson TM, Boyd RD, Platt HS, Strang LB: Composition of alveolar liquid in the foetal lamb. J Physiol 1969, 204(1):159-168.
- [49]Tate S, MacGregor G, Davis M, Innes JA, Greening AP: Airways in cystic fibrosis are acidified: detection by exhaled breath condensate. Thorax 2002, 57(11):926-929.
- [50]Ricciardolo FL, Gaston B, Hunt J: Acid stress in the pathology of asthma. J Allergy Clin Immunol 2004, 113(4):610-619.
- [51]Bekku S, Mochizuki H, Yamamoto T, Ueno H, Takayama E, Tadakuma T: Expression of carbonic anhydrase I or II and correlation to clinical aspects of colorectal cancer. Hepatogastroenterology 2000, 47(34):998-1001.
- [52]Leppilampi M, Koistinen P, Savolainen ER, Hannuksela J, Parkkila AK, Niemela O, Pastorekova S, Pastorek J, Waheed A, Sly WS, et al.: The expression of carbonic anhydrase II in hematological malignancies. Clin Cancer Res 2002, 8(7):2240-2245.
- [53]Chiche J, Ilc K, Laferriere J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, Pouyssegur J: Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res 2009, 69(1):358-368.
- [54]Brockton NT, Klimowicz AC, Bose P, Petrillo SK, Konno M, Rudmik L, Dean M, Nakoneshny SC, Matthews TW, Chandarana S, et al.: High stromal carbonic anhydrase IX expression is associated with nodal metastasis and decreased survival in patients with surgically-treated oral cavity squamous cell carcinoma. Oral Oncol 2012, 48(7):615-622.
- [55]Parkkila S, Parkkila AK, Saarnio J, Kivela J, Karttunen TJ, Kaunisto K, Waheed A, Sly WS, Tureci O, Virtanen I, et al.: Expression of the membrane-associated carbonic anhydrase isozyme XII in the human kidney and renal tumors. J Histochem Cytochem 2000, 48(12):1601-1608.
- [56]Kummola L, Hamalainen JM, Kivela J, Kivela AJ, Saarnio J, Karttunen T, Parkkila S: Expression of a novel carbonic anhydrase, CA XIII, in normal and neoplastic colorectal mucosa. BMC cancer 2005, 5:41. BioMed Central Full Text
- [57]Swietach P, Wigfield S, Cobden P, Supuran CT, Harris AL, Vaughan-Jones RD: Tumor-associated carbonic anhydrase 9 spatially coordinates intracellular pH in three-dimensional multicellular growths. J Biol Chem 2008, 283(29):20473-20483.
- [58]Williams E, Martin S, Moss R, Durrant L, Deen S: Co-expression of VEGF and CA9 in ovarian high-grade serous carcinoma and relationship to survival. Virchows Arch 2012, 461(1):33-39.
- [59]Shin HJ, Rho SB, Jung DC, Han IO, Oh ES, Kim JY: Carbonic anhydrase IX (CA9) modulates tumor-associated cell migration and invasion. J Cell Sci 2011, 124(Pt 7):1077-1087.
- [60]Parkkila S, Rajaniemi H, Parkkila AK, Kivela J, Waheed A, Pastorekova S, Pastorek J, Sly WS: Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci U S A 2000, 97(5):2220-2224.
- [61]Zatovicova M, Jelenska L, Hulikova A, Csaderova L, Ditte Z, Ditte P, Goliasova T, Pastorek J, Pastorekova S: Carbonic anhydrase IX as an anticancer therapy target: preclinical evaluation of internalizing monoclonal antibody directed to catalytic domain. Curr Pharm Des 2010, 16(29):3255-3263.
- [62]Muselaers S, Mulders P, Oosterwijk E, Oyen W, Boerman O: Molecular imaging and carbonic anhydrase IX-targeted radioimmunotherapy in clear cell renal cell carcinoma. Immunotherapy 2013, 5(5):489-495.
- [63]Oosterwijk-Wakka JC, Boerman OC, Mulders PF, Oosterwijk E: Application of Monoclonal Antibody G250 Recognizing Carbonic Anhydrase IX in Renal Cell Carcinoma. Int J Mol Sci 2013, 14(6):11402-11423.
- [64]Tjäderhane L, Larjava H, Sorsa T, Uitto VJ, Larmas M, Salo T: The activation and function of host matrix metalloproteinases in dentin matrix breakdown in caries lesions. J Dent Res 1998, 77(8):1622-1629.
- [65]Davis GE, Martin BM: A latent Mr 94,000 gelatin-degrading metalloprotease induced during differentiation of HL-60 promyelocytic leukemia cells: a member of the collagenase family of enzymes. Cancer Res 1990, 50(4):1113-1120.
- [66]Davis GE: Identification of an abundant latent 94-kDa gelatin-degrading metalloprotease in human saliva which is activated by acid exposure: implications for a role in digestion of collagenous proteins. Arch Biochem Biophys 1991, 286(2):551-554.
- [67]Martinez-Zaguilan R, Seftor EA, Seftor RE, Chu YW, Gillies RJ, Hendrix MJ: Acidic pH enhances the invasive behavior of human melanoma cells. Clin Exp Metastasis 1996, 14(2):176-186.
- [68]Karsdal MA, Henriksen K, Sorensen MG, Gram J, Schaller S, Dziegiel MH, Heegaard AM, Christophersen P, Martin TJ, Christiansen C, et al.: Acidification of the osteoclastic resorption compartment provides insight into the coupling of bone formation to bone resorption. Am J Pathol 2005, 166(2):467-476.
- [69]Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, Moritz JD, Schu P, Von Figura K: Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A 1998, 95(23):13453-13458.
- [70]Le Gall C, Bellahcene A, Bonnelye E, Gasser JA, Castronovo V, Green J, Zimmermann J, Clezardin P: A cathepsin K inhibitor reduces breast cancer induced osteolysis and skeletal tumor burden. Cancer Res 2007, 67(20):9894-9902.
- [71]Podgorski I, Linebaugh BE, Koblinski JE, Rudy DL, Herroon MK, Olive MB, Sloane BF: Bone marrow-derived cathepsin K cleaves SPARC in bone metastasis. Am J Pathol 2009, 175(3):1255-1269.
- [72]Nakajima M, Irimura T, Di Ferrante D, Di Ferrante N, Nicolson GL: Heparan sulfate degradation: relation to tumor invasive and metastatic properties of mouse B16 melanoma sublines. Science 1983, 220(4597):611-613.
- [73]Nakajima M, Irimura T, Di Ferrante N, Nicolson GL: Metastatic melanoma cell heparanase. Characterization of heparan sulfate degradation fragments produced by B16 melanoma endoglucuronidase. J Biol Chem 1984, 259(4):2283-2290.
- [74]Kato Y, Ozawa S, Tsukuda M, Kubota E, Miyazaki K, St-Pierre Y, Hata R: Acidic extracellular pH increases calcium influx-triggered phospholipase D activity along with acidic sphingomyelinase activation to induce matrix metalloproteinase-9 expression in mouse metastatic melanoma. FEBS J 2007, 274(12):3171-3183.
- [75]Kato Y, Nakayama Y, Umeda M, Miyazaki K: Induction of 103-kDa gelatinase/type IV collagenase by acidic culture conditions in mouse metastatic melanoma cell lines. J Biol Chem 1992, 267(16):11424-11430.
- [76]Griffiths L, Dachs GU, Bicknell R, Harris AL, Stratford IJ: The influence of oxygen tension and pH on the expression of platelet-derived endothelial cell growth factor/thymidine phosphorylase in human breast tumor cells grown in vitro and in vivo. Cancer Res 1997, 57(4):570-572.
- [77]Bellocq A, Suberville S, Philippe C, Bertrand F, Perez J, Fouqueray B, Cherqui G, Baud L: Low environmental pH is responsible for the induction of nitric-oxide synthase in macrophages. Evidence for involvement of nuclear factor-κB activation. J Biol Chem 1998, 273(9):5086-5092.
- [78]Fukumura D, Xu L, Chen Y, Gohongi T, Seed B, Jain RK: Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res 2001, 61(16):6020-6024.
- [79]Xu L, Fukumura D, Jain RK: Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF. J Biol Chem 2002, 277(13):11368-11374.
- [80]Shi Q, Abbruzzese JL, Huang S, Fidler IJ, Xiong Q, Xie K: Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic. Clin Cancer Res 1999, 5(11):3711-3721.
- [81]Shi Q, Le X, Wang B, Xiong Q, Abbruzzese JL, Xie K: Regulation of interleukin-8 expression by cellular pH in human pancreatic adenocarcinoma cells. J Interferon Cytokine Res 2000, 20(11):1023-1028.
- [82]Shi Q, Xiong Q, Le X, Xie K: Regulation of interleukin-8 expression by tumor-associated stress factors. J Interferon Cytokine Res 2001, 21(8):553-566.
- [83]Xu L, Fidler IJ: Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells. Cancer Res 2000, 60(16):4610-4616.
- [84]Shi Q, Le X, Wang B, Abbruzzese JL, Xiong Q, He Y, Xie K: Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells. Oncogene 2001, 20(28):3751-3756.
- [85]Bischoff DS, Zhu JH, Makhijani NS, Yamaguchi DT: Acidic pH stimulates the production of the angiogenic CXC chemokine, CXCL8 (interleukin-8), in human adult mesenchymal stem cells via the extracellular signal-regulated kinase, p38 mitogen-activated protein kinase, and NF-κB pathways. J Cell Biochem 2008, 104(4):1378-1392.
- [86]Kato Y, Ozono S, Shuin T, Miyazaki K: Slow induction of gelatinase B mRNA by acidic culture conditions in mouse metastatic melanoma cells. Cell Biol Int 1996, 20(5):375-377.
- [87]Kato Y, Lambert CA, Colige AC, Mineur P, Noël A, Frankenne F, Foidart JM, Baba M, Hata RI, Miyazaki K, et al.: Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J Biol Chem 2005, 280(12):10938-10944.
- [88]Itatsu K, Sasaki M, Harada K, Yamaguchi J, Ikeda H, Sato Y, Ohta T, Sato H, Nagino M, Nimura Y, et al.: Phosphorylation of extracellular signal-regulated kinase 1/2, p38 mitogen-activated protein kinase and nuclear translocation of nuclear factor-κB are involved in upregulation of matrix metalloproteinase-9 by tumour necrosis factor-α. Liver Int 2009, 29(2):291-298.
- [89]Hirata S, Fukamachi T, Sakano H, Tarora A, Saito H, Kobayashi H: Extracellular acidic environments induce phosphorylation of ZAP-70 in Jurkat T cells. Immunol Lett 2008, 115(2):105-109.
- [90]Tomura H, Wang JQ, Komachi M, Damirin A, Mogi C, Tobo M, Kon J, Misawa N, Sato K, Okajima F: Prostaglandin l2 production and cAMP accumulation in response to acidic extracellular pH through OGR1 in human aortic smooth muscle cells. J Biol Chem 2005, 280(41):34458-34464.
- [91]Torigoe T, Izumi H, Yoshida Y, Ishiguchi H, Okamoto T, Itoh H, Kohno K: Low pH enhances Sp1 DNA binding activity and interaction with TBP. Nucleic Acids Res 2003, 31(15):4523-4530.
- [92]Chen Y, Chen CH, Tung PY, Huang SH, Wang SM: An acidic extracellular pH disrupts adherens junctions in HepG2 cells by Src kinases-dependent modification of E-cadherin. J Cell Biochem 2009, 108(4):851-859.
- [93]Chen Y, Kung HN, Chen CH, Huang SH, Chen KH, Wang SM: Acidic extracellular pH induces p120-catenin-mediated disruption of adherens junctions via the Src kinase-PKCδ pathway. FEBS Lett 2011, 585(4):705-710.
- [94]Bourguignon LY, Singleton PA, Diedrich F, Stern R, Gilad E: CD44 interaction with Na+-H+ exchanger (NHE1) creates acidic microenvironments leading to hyaluronidase-2 and cathepsin B activation and breast tumor cell invasion. J Biol Chem 2004, 279(26):26991-27007.
- [95]Mori H, Tomari T, Koshikawa N, Kajita M, Itoh Y, Sato H, Tojo H, Yana I, Seiki M: CD44 directs membrane-type 1 matrix metalloproteinase to lamellipodia by associating with its hemopexin-like domain. EMBO J 2002, 21(15):3949-3959.
- [96]Suenaga N, Mori H, Itoh Y, Seiki M: CD44 binding through the hemopexin-like domain is critical for its shedding by membrane-type 1 matrix metalloproteinase. Oncogene 2005, 24(5):859-868.
- [97]Lin Y, Chang G, Wang J, Jin W, Wang L, Li H, Ma L, Li Q, Pang T: NHE1 mediates MDA-MB-231 cells invasion through the regulation of MT1-MMP. Exp Cell Res 2011, 317(14):2031-2040.
- [98]Lin Y, Wang J, Jin W, Wang L, Li H, Ma L, Li Q, Pang T: NHE1 mediates migration and invasion of HeLa cells via regulating the expression and localization of MT1-MMP. Cell Biochem Funct 2012, 1:41-46.
- [99]Robey IF, Baggett BK, Kirkpatrick ND, Roe DJ, Dosescu J, Sloane BF, Hashim AI, Morse DL, Raghunand N, Gatenby RA, et al.: Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res 2009, 69(6):2260-2268.
- [100]Lora-Michiels M, Yu D, Sanders L, Poulson JM, Azuma C, Case B, Vujaskovic Z, Thrall DE, Charles HC, Dewhirst MW: Extracellular pH and P-31 magnetic resonance spectroscopic variables are related to outcome in canine soft tissue sarcomas treated with thermoradiotherapy. Clin Cancer Res 2006, 12(19):5733-5740.
- [101]Berdiev BK, Xia J, McLean LA, Markert JM, Gillespie GY, Mapstone TB, Naren AP, Jovov B, Bubien JK, Ji HL, et al.: Acid-sensing ion channels in malignant gliomas. J Biol Chem 2003, 278(17):15023-15034.
- [102]Ohta T, Imagawa T, Ito S: Novel gating and sensitizing mechanism of capsaicin receptor (TRPV1): tonic inhibitory regulation of extracellular sodium through the external protonation sites on TRPV1. J Biol Chem 2008, 283(14):9377-9387.
- [103]Nakaya K, Harbidge DG, Wangemann P, Schultz BD, Green ED, Wall SM, Marcus DC: Lack of pendrin HCO3- transport elevates vestibular endolymphatic [Ca2+] by inhibition of acid-sensitive TRPV5 and TRPV6 channels. Am J Physiol Renal Physiol 2007, 292(5):F1314-F1321.
- [104]Chen Y, Willcockson HH, Valtschanoff JG: Vanilloid receptor TRPV1-mediated phosphorylation of ERK in murine adjuvant arthritis. Osteoarthritis Cartilage 2009, 17(2):244-251.
- [105]Chen Y, Williams SH, McNulty AL, Hong JH, Lee SH, Rothfusz NE, Parekh PK, Moore C, Gereau RW, Taylor AB, et al.: Temporomandibular joint pain: A critical role for Trpv4 in the trigeminal ganglion. Pain 2013, 154(8):1295-1304.
- [106]Wang G, Su J, Li L, Feng J, Shi L, He W, Liu Y: Edaravone alleviates hypoxia-acidosis/reoxygenation-induced neuronal injury by activating ERK1/2. Neurosci Lett 2013, 543:72-77.
- [107]Numata T, Okada Y: Proton conductivity through the human TRPM7 channel and its molecular determinants. J Biol Chem 2008, 283(22):15097-15103.
- [108]Davis FM, Azimi I, Faville RA, Peters AA, Jalink K, Putney JW Jr, Goodhill GJ, Thompson EW, Roberts-Thomson SJ, Monteith GR: Induction of epithelial-mesenchymal transition (EMT) in breast cancer cells is calcium signal dependent. Oncogene 2013. in press
- [109]Stüwe L, Müller M, Fabian A, Waning J, Mally S, Noël J, Schwab A, Stock C: pH dependence of melanoma cell migration: protons extruded by NHE1 dominate protons of the bulk solution. J Physiol 2007, 585(Pt 2):351-360.
- [110]Tominaga T, Barber DL: Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading. Mol Biol Cell 1998, 9(8):2287-2303.
- [111]Denker SP, Barber DL: Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 2002, 159(6):1087-1096.
- [112]Stock C, Gassner B, Hauck CR, Arnold H, Mally S, Eble JA, Dieterich P, Schwab A: Migration of human melanoma cells depends on extracellular pH and Na+/H+ exchange. J Physiol 2005, 567(Pt 1):225-238.
- [113]Krahling H, Mally S, Eble JA, Noel J, Schwab A, Stock C: The glycocalyx maintains a cell surface pH nanoenvironment crucial for integrin-mediated migration of human melanoma cells. Pflugers Arch 2009, 458(6):1069-1083.
- [114]Cardone RA, Casavola V, Reshkin SJ: The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nat Rev Cancer 2005, 5(10):786-795.
- [115]Montcourrier P, Silver I, Farnoud R, Bird I, Rochefort H: Breast cancer cells have a high capacity to acidify extracellular milieu by a dual mechanism. Clin Exp Metastasis 1997, 15(4):382-392.
- [116]Chi SL, Pizzo SV: Angiostatin is directly cytotoxic to tumor cells at low extracellular pH: a mechanism dependent on cell surface-associated ATP synthase. Cancer Res 2006, 66(2):875-882.
- [117]Spugnini EP, Citro G, Fais S: Proton pump inhibitors as anti vacuolar-ATPases drugs: a novel anticancer strategy. J Exp Clin Cancer Res 2010, 29:44. BioMed Central Full Text
- [118]De Milito A, Canese R, Marino ML, Borghi M, Iero M, Villa A, Venturi G, Lozupone F, Iessi E, Logozzi M, et al.: pH-dependent antitumor activity of proton pump inhibitors against human melanoma is mediated by inhibition of tumor acidity. Int J Cancer 2010, 127(1):207-219.
- [119]Wiedmann RM, Von Schwarzenberg K, Palamidessi A, Schreiner L, Kubisch R, Liebl J, Schempp C, Trauner D, Vereb G, Zahler S, et al.: The V-ATPase-inhibitor archazolid abrogates tumor metastasis via inhibition of endocytic activation of the Rho-GTPase Rac1. Cancer Res 2012, 72(22):5976-5987.
- [120]Adams DJ, Dewhirst MW, Flowers JL, Gamcsik MP, Colvin OM, Manikumar G, Wani MC, Wall ME: Camptothecin analogues with enhanced antitumor activity at acidic pH. Cancer Chemother Pharmacol 2000, 46(4):263-271.
- [121]Vukovic V, Tannock IF: Influence of low pH on cytotoxicity of paclitaxel, mitoxantrone and topotecan. Br J Cancer 1997, 75(8):1167-1172.
- [122]Raghunand N, He X, Van Sluis R, Mahoney B, Baggett B, Taylor CW, Paine-Murrieta G, Roe D, Bhujwalla ZM, Gillies RJ: Enhancement of chemotherapy by manipulation of tumour pH. Br J Cancer 1999, 80(7):1005-1011.
- [123]Raghunand N, Mahoney B, Van Sluis R, Baggett B, Gillies RJ: Acute metabolic alkalosis enhances response of C3H mouse mammary tumors to the weak base mitoxantrone. Neoplasia 2001, 3(3):227-235.
- [124]Lotz C, Kelleher DK, Gassner B, Gekle M, Vaupel P, Thews O: Role of the tumor microenvironment in the activity and expression of the p-glycoprotein in human colon carcinoma cells. Oncol Rep 2007, 17(1):239-244.
- [125]Thews O, Dillenburg W, Rosch F, Fellner M: PET imaging of the impact of extracellular pH and MAP kinases on the p-glycoprotein (Pgp) activity. Adv Exp Med Biol 2013, 765:279-286.
- [126]Ko J, Park K, Kim YS, Kim MS, Han JK, Kim K, Park RW, Kim IS, Song HK, Lee DS, et al.: Tumoral acidic extracellular pH targeting of pH-responsive MPEG-poly(β-amino ester) block copolymer micelles for cancer therapy. J Control Release 2007, 123(2):109-115.
- [127]Lee ES, Gao Z, Kim D, Park K, Kwon IC, Bae YH: Super pH-sensitive multifunctional polymeric micelle for tumor pHe specific TAT exposure and multidrug resistance. J Control Release 2008, 129(3):228-236.
- [128]Garcia-Martin ML, Martinez GV, Raghunand N, Sherry AD, Zhang S, Gillies RJ: High resolution pHe imaging of rat glioma using pH-dependent relaxivity. Magn Reson Med 2006, 55(2):309-315.
- [129]Van Sluis R, Bhujwalla ZM, Raghunand N, Ballesteros P, Alvarez J, Cerdan S, Galons JP, Gillies RJ: In vivo imaging of extracellular pH using 1H MRSI. Magn Reson Med 1999, 41(4):743-750.
- [130]Adachi E, Tannock IF: The effects of vasodilating drugs on pH in tumors. Oncol Res 1999, 11(4):179-185.
- [131]Raghunand N, Mahoney BP, Gillies RJ: Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol 2003, 66(7):1219-1229.
- [132]Betof AS, Rabbani ZN, Hardee ME, Kim SJ, Broadwater G, Bentley RC, Snyder SA, Vujaskovic Z, Oosterwijk E, Harris LN, et al.: Carbonic anhydrase IX is a predictive marker of doxorubicin resistance in early-stage breast cancer independent of HER2 and TOP2A amplification. Br J Cancer 2012, 106(5):916-922.
- [133]Teh BG, Kobayashi W, Narita K, Fukui R, Kimura H: Superselective docetaxel-nedaplatin combined infusion concurrent with radiation thrapy in advanced oral cancers. Oral Oncol EXTRA 2004, 40:126-131.
- [134]Shiga K, Yokoyama J, Hashimoto S, Saijo S, Tateda M, Ogawa T, Watanabe M, Kobayashi T: Combined therapy after superselective arterial cisplatin infusion to treat maxillary squamous cell carcinoma. Otolaryngol Head Neck Surg 2007, 136(6):1003-1009.
- [135]Overgaard J, Bichel P: The influence of hypoxia and acidity on the hyperthermic response of malignant cells in vitro. Radiology 1977, 123(2):511-514.
- [136]Coss RA, Storck CW, Daskalakis C, Berd D, Wahl ML: Intracellular acidification abrogates the heat shock response and compromises survival of human melanoma cells. Mol Cancer Ther 2003, 2(4):383-388.
- [137]Coss RA, Storck CW, Wachsberger PR, Reilly J, Leeper DB, Berd D, Wahl ML: Acute extracellular acidification reduces intracellular pH, 42°C-induction of heat shock proteins and clonal survival of human melanoma cells grown at pH 6.7. Int J Hyperthermia 2004, 20(1):93-106.
- [138]Lan A, Lagadic-Gossmann D, Lemaire C, Brenner C, Jan G: Acidic extracellular pH shifts colorectal cancer cell death from apoptosis to necrosis upon exposure to propionate and acetate, major end-products of the human probiotic propionibacteria. Apoptosis 2007, 12(3):573-591.