Cell surface F1/Fo ATP synthase contributes to interstitial flow-mediated development of the acidic microenvironment in tumor tissues

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 11, 2013, Pages

  Kawai, Yoshiko ^a   Kaidoh, Maki ^a   Yokoyama, Yumiko ^a   Ohhashi, Toshio ^a  

^a SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

ATPase; Bafilomycin A; Carbonic anhydrase IX; CO2 gas excretion; Corelease of ATP and H+; MDA MB 231; Piceatannol

Indexed keywords

ACETAZOLAMIDE; ADENOSINE TRIPHOSPHATE; ANGIOSTATIN; BAFILOMYCIN; CARBON DIOXIDE; CARBONATE DEHYDRATASE IX; ECTONUCLEOSIDE TRIPHOSPHATE DIPHOSPHOHYDROLASE 3; ENZYME; LACTIC ACID; MESSENGER RNA; OMEPRAZOLE; PICEATANNOL; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PURINERGIC P2Y1 RECEPTOR; UNCLASSIFIED DRUG; BAFILOMYCIN A; ENZYME INHIBITOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ACIDITY; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL CULTURE; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME RELEASE; FLUID FLOW; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTERSTITIAL FLUID; MELANOMA CELL; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SHEAR STRESS; TUMOR MICROENVIRONMENT; BIOSYNTHESIS; CARBONIC ANHYDRASE IX, ATPASE; CELL MEMBRANE; CO2 GAS EXCRETION; CORELEASE OF ATP AND H+; CULTURE TECHNIQUE; DRUG ANTAGONISM; ENZYMOLOGY; EXTRACELLULAR FLUID; MDA-MB-231; METHODOLOGY; PH; PHYSIOLOGY; SHEAR STRENGTH; TUMOR CELL LINE; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; PROCEDURES;

BAFILOMYCIN A; CARBONIC ANHYDRASE IX, ATPASE; CO2 GAS EXCRETION; CORELEASE OF ATP AND H+; MDA-MB-231; PICEATANNOL;

CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL MEMBRANE; ENZYME INHIBITORS; EXTRACELLULAR FLUID; HUMANS; HYDROGEN-ION CONCENTRATION; PROTON-TRANSLOCATING ATPASES; SHEAR STRENGTH; TUMOR MICROENVIRONMENT;

EID: 84888813332     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00199.2013     Document Type: Article

References (38)

1. Baish JW, Netti PA, Jain RK. Transmural coupling of fluid flow in microcirculatory network and interstitium in tumors. Microvasc Res 53: 128-141, 1997.
2. Bissell MJ, Jines WC. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 17: 320-339, 2011.
3. Bulanova E, Bulfone-Paus S. P2 receptor-mediated signaling in mast cell biology. Purinergic Signal 6: 3-17, 2010.
4. Cahoon L. Let's get physical mechanical forces drive a new field of study. Nat Med 17: 271, 2011.
5. Chien S. Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292: H1209-H1224, 2007.
6. 2 reactions. J Clin Invest 62: 618-622, 1978.
7. Crawford PA, Gaddie KJ, Smith TM, Kirley TL. Characterization of an alternative splice variant of human nucleoside triphosphate diphosphohydrolase 3 (NTPDase 3): a possible modulator of nucleotidase activity and purinergic signaling. Arch Biochem Biophys 457: 7-15, 2007.
8. Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev 75: 519-560, 1995.
9. Ebbesen P, Pettersen EO, Gorr TA, Jobst G, Williams K, Kieninger J, Wenger RH, Pastorekova S, Dubois L, Lambin P, Wouters BG, Van Den Beucken T, Supuran CT, Poellinger L, Ratcliffe P, Kanopka A, Görlach A, Gasmann M, Harris AL, Maxwell P, Scozzafava A. Taking advantage of tumor cell adaptations to hypoxia for developing new tumor markers and treatment strategies. J Enzyme Inhib Med Chem 24: 1-39, 2009.
10. Fais S. Proton pump inhibitor-induced tumor cell death by inhibition of a detoxification mechanism. J Intern Med 267: 515-525, 2010.
11. Fukaya Y, Ohhashi T. Acetylcholine-and flow-induced production and release of nitric oxide in arterial and venous endothelial cells. Am J Physiol Heart Circ Physiol 270: H99-H106, 1996.
12. Fukumura D, Jain RK. Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc Res 74: 72-84, 2007.
13. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4: 891-899, 2004.
14. Hilvo M, Baranauskiene L, Salzano AM, Scaloni A, Matulis D, Innocenti A, Scozzafava A, Monti SM, Di Fiore A, De Simone G, Lindfors M, Jänis J, Valjakka J, Pastoreková S, Pastorek J, Kulomaa MS, Nordlund HR, Supuran CT, Parkkila S. Biochemical characterization of CA IX: one of the most active carbonic anhydrase isozymes. J Biol Chem 283: 27799-27809, 2008.
15. Hinton A, Sennoune SR, Bond S, Fang M, Reuveni M, Sahagian GG, Jay D, Martinez-Zaguilan R, Forgac M. Function of a subunit isoforms of the V-ATPase in pH homeostasis and in vitro invasion of NDA-MB231 human breast cancer cells. J Biol Chem 284: 16400-16408, 2009.
16. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2: 289-300, 2002.
17. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumor-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 8: 1369-1375, 2006.
18. Jain RK. Delivery of molecular and cellular medicine to solid tumors. Microcirculation 4: 1-23, 1997.
19. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438: 820-827, 2005.
20. Kawai Y, Yokoyama Y, Kaidoh M, Ohhashi T. Shear stress-induced ATP-mediated endothelial constitutive nitric oxide synthase expression in human lymphatic endothelial cells. Am J Physiol Cell Physiol 298: C647-C655, 2010.
21. 2 gas excretion from human pulmonary arteriolar endothelial cells. J Cell Physiol 227: 2059-2068, 2012.
22. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13: 472-482, 2008.
23. Lopez-Castejón G, Baroja-Mazo A, Pelegrín P. Novel macrophage polarization model: from gene expression to identification of new antiinflammatory molecules. Cell Mol Life Sci 68: 3095-3107, 2011.
24. Lu DJ, Grinstein S. ATP and guanine nucleotide dependence of neutrophil activation. Evidence for the involvement of two distinct GTP-binding proteins. J Biol Chem 265: 13721-13729, 1990.
25. Marcus AJ, Broekman MJ, Drosopoulos JH, Islam N, Pinsky DJ, Sesti C, Levi R. Metabolic control of excessive extracellular nucleotide accumulation by CD 39/ecto-nucleotidase-1: Implications for ischemic vascular diseases. J Pharmacol Exp Ther 305: 9-16, 2003.
26. Moser TL, Kenan DJ, Ashley TA, Roy JA, Goodman MD, Misra UK, Cheek DJ, Pizzo SV. Endothelial cell surface F1-FO ATP synthase is active in ATP synthesis and is inhibited by angiostatin. Proc Natl Acad Sci USA 98: 6656-6661, 2001.
27. Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 10: 767-777, 2011.
28. Ohhashi T, Mizuno R, Ikomi F, Kawai Y. Current topics of physiology and pharmacology in the lymphatic system. Pharmacol Ther 105: 165-188, 2005.
29. Palumbo R, Gaetano C, Melillo G, Toschi E, Remuzzi A, Capogrossi MC. Shear stress downregulation of platelet-derived growth factor receptor-beta and matrix metalloprotease-2 is associated with inhibition of smooth muscle cell invasion and migration. Circulation 102: 225-230, 2000.
30. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM. Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254, 2005.
31. Pelegrín P, Surprenant A. Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1beta release through pyrophosphate. EMBO J 28: 2114-2127, 2009.
32. Pouyssegur J, Dayan F, Mazure NM. Hypoxia signaling in cancer and approaches to enforce tumour regression. Nature 441: 437-443, 2006.
33. Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 7: 168-181, 2008.
34. Svastová E, Hulíková A, Rafajová M, Zat'ovicová M, Gibadulinová A, Casini A, Cecchi A, Scozzafava A, Supuran CT, Pastorek J, Pastoreková S. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 577: 439-445, 2004.
35. 2 selectively inhibits interleukin-6 and tumor necrosis factor expression and decreases phagocytosis in the macrophage. FASEB J 24: 2178-2190, 2010.
36. Wykoff CC, Beasley NJP, Watson PM, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60: 7075-7083, 2000.
37. Yamamoto K, Shimizu N, Obi S, Kumagaya S, Taketani Y, Kamiya A, Ando J. Involvement of cell surface ATP synthase in flow-induced ATP release by vascular endothelial cells. Am J Physiol Heart Circ Physiol 293: H1646-H1653, 2007.
38. Yashiro Y, Ohhashi T. Flow-and agonist-mediated nitric oxide-and prostaglandin-dependent dilation in spinal arteries. Am J Physiol Heart Circ Physiol 273: H2217-H2223, 1997.