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 Journal

Volumn 274, Issue 12, 2007, Pages 3171-3183

  Kato, Yasumasa ^a,b   Ozawa, Shigeyuki ^a   Tsukuda, Mamoru ^b   Kubota, Eiro ^a   Miyazaki, Kaoru ^c   St Pierre, Yves ^d   Hata, Ryu Ichiro ^a  

^a KANAGAWA DENTAL COLLEGE   (Japan)

^b YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

Acidic sphingomylinase; Ca2+ influx; Extracellular acidic pH; MMP 9

Indexed keywords

CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL T TYPE; CHELATING AGENT; DESIPRAMINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FANTOFARONE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MIBEFRADIL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PERHEXILINE; PHOSPHOLIPASE D; SMALL INTERFERING RNA; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; VOLTAGE GATED CALCIUM CHANNEL;

ACIDITY; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL PH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXTRACELLULAR SPACE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CELL LINE, TUMOR; CHELATING AGENTS; DESIPRAMINE; EGTAZIC ACID; ENZYME ACTIVATION; EXTRACELLULAR FLUID; HYDROGEN-ION CONCENTRATION; INDOLIZINES; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 9; MELANOMA; MIBEFRADIL; MICE; NF-KAPPA B; NIMODIPINE; PERHEXILINE; PHENETHYLAMINES; PHOSPHOLIPASE D; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 34249790593     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05848.x     Document Type: Article

References (64)

1. Raghunand N Gillies RJ (2001) pH and chemotherapy. Novartis Found Symp 240, 199 211 discussion 265 198.
2. Lora-Michiels M, Yu D, Sanders L, Poulson JM, Azuma C, Case B, Vujaskovic Z, Thrall DE, Charles HC Dewhirst MW (2006) Extracellular pH and P-31 magnetic resonance spectroscopic variables are related to outcome in canine soft tissue sarcomas treated with thermoradiotherapy. Clin Cancer Res 12, 5733 5740.
3. Shi Q, Abbruzzese JL, Huang S, Fidler IJ, Xiong Q Xie K (1999) Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic. Clin Cancer Res 5, 3711 3721.
4. Xu L Fidler IJ (2000) Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells. Cancer Res 60, 4610 4616.
5. Shi Q, Xiong Q, Le X Xie K (2001) Regulation of interleukin-8 expression by tumor-associated stress factors. J Interferon Cytokine Res 21, 553 566.
6. Fukumura D, Xu L, Chen Y, Gohongi T, Seed B Jain RK (2001) Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res 61, 6020 6024.
7. Xu L, Fukumura D Jain RK (2002) 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 277, 11368 11374.
8. Yamaguchi A, Tojyo I, Yoshida H Fujita S (2005) Role of hypoxia and interleukin-1β in gene expressions of matrix metalloproteinases in temporomandibular joint disc cells. Arch Oral Biol 50, 81 87.
9. Kato Y, Nakayama Y, Umeda M Miyazaki K (1992) Induction of 103-kDa gelatinase/type IV collagenase by acidic culture conditions in mouse metastatic melanoma cell lines. J Biol Chem 267, 11424 11430.
10. Kato Y, Lambert CA, Colige AC, Mineur P, Noël A, Frankenne F, Foidart JM, Baba M, Hata RI, Miyazaki K et al. (2005) 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 280, 10938 10944.
11. Smith JB, Dwyer SD Smith L (1989) Lowering extracellular pH evokes inositol polyphosphate formation and calcium mobilization. J Biol Chem 264, 8723 8728.
12. Dwyer SD, Zhuang Y Smith JB (1991) Calcium mobilization by cadmium or decreasing extracellular Na+ or pH in coronary endothelial cells. Exp Cell Res 192, 22 31.
13. Batlle DC, Peces R, LaPointe MS, YeM Daugirdas JT (1993) Cytosolic free calcium regulation in response to acute changes in intracellular pH in vascular smooth muscle. Am J Physiol 264, C932 C943.
14. Iwasawa K, Nakajima T, Hazama H, Goto A, Shin WS, Toyo-oka T Omata M (1997) Effects of extracellular pH on receptor-mediated Ca2+ influx in A7r5 rat smooth muscle cells: involvement of two different types of channel. J Physiol 503, 237 251.
15. Tomura H, Wang JQ, Komachi M, Damirin A, Mogi C, Tobo M, Kon J, Misawa N, Sato K Okajima F (2005) Prostaglandin l2 production and cAMP accumulation in response to acidic extracellular pH through OGR1 in human aortic smooth muscle cells. J Biol Chem 280, 34458 34464.
16. Bourgoin SG, Harbour D Poubelle PE (1996) Role of protein kinase Cα, Arf, and cytoplasmic calcium transients in phospholipase D activation by sodium fluoride in osteoblast-like cells. J Bone Miner Res 11, 1655 1665.
17. Caumont AS, Galas MC, Vitale N, Aunis D Bader MF (1998) Regulated exocytosis in chromaffin cells. Translocation of ARF6 stimulates a plasma membrane-associated phospholipase D. J Biol Chem 273, 1373 1379.
18. Higuchi M, Singh S, Jaffrézou J-P Aggarwal BB (1996) Acidic sphingomyelinase-generated ceramide is needed but not sufficient for TNF-induced apoptosis and nuclear factor-κB activation. J Immunol 157, 297 304.
19. Saldeen J, Jaffrézou J-P Welsh N (2000) The acid sphingomyelinase inhibitor SR33557 counteracts TNF-α-mediated potentiation of IL-1β-induced NF-κB activation in the insulin-producing cell line Rinm5F. Autoimmunity 32, 241 254.
20. Bond M, Fabunmi RP, Baker AH Newby AC (1998) Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-κB. FEBS Lett 435, 29 34.
21. Colell A, Morales A, Fernández-Checa JC García-Ruiz C (2002) Ceramide generated by acidic sphingomyelinase contributes to tumor necrosis factor-α-mediated apoptosis in human colon HT-29 cells through glycosphingolipids formation. Possible role of ganglioside GD3. FEBS Lett 526, 135 141.
22. Pru JK, Hendry IR, Davis JS Rueda BR (2002) Soluble Fas ligand activates the sphingomyelin pathway and induces apoptosis in luteal steroidogenic cells independently of stress-activated p38 (MAPK). Endocrinology 143, 4350 4357.
23. Fleenor DL, Pang IH Clark AF (2003) Involvement of AP-1 in interleukin-1α-stimulated MMP-3 expression in human trabecular meshwork cells. Invest Ophthalmol Vis Sci 44, 3494 3501.
24. Chung HS, Park SR, Choi EK, Park HJ, Griffin RJ, Song CW Park H (2003) Role of sphingomyelin-MAPKs pathway in heat-induced apoptosis. Exp Mol Med 35, 181 188.
25. Czarny M, Liu J, Oh P Schnitzer JE (2003) Transient mechanoactivation of neutral sphingomyelinase in caveolae to generate ceramide. J Biol Chem 278, 4424 4430.
26. Reunanen N, Westermarck J, Hakkinen L, Holmström TH, Elo I, Eriksson JE Kähäri VM (1998) Enhancement of fibroblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stress-activated protein kinase pathways. J Biol Chem 273, 5137 5145.
27. Buisson-Legendre N, Bernard P, Bobichon H, Emonard H, Schneider C, Maquart FX, Haye B Hornebeck W (1999) Involvement of the 92-kDa gelatinase (matrix metalloproteinase-9) in the ceramide-mediated inhibition of human keratinocyte growth. Biochem Biophys Res Commun 260, 634 640.
28. Romey G, Bois P Lazdunski M (1994) Effects of two chemically related new Ca2+ channel antagonists, SR33557 (fantofarone) and SR33805, on the L-type cardiac channel. Eur J Pharmacol 263, 101 105.
29. Yasui K Palade P (1995) Inhibitory action of SR33557 on L-type calcium current in single ventricular myocytes of rat. Br J Pharmacol 114, 468 474.
30. Jaffrézou J-P, Levade T, Kuhlein E, Thurneyssen O, Chiron M, Grandjean H, Carrière D Laurent G (1990) Enhancement of ricin A chain immunotoxin activity by perhexiline on established and fresh leukemic cells. Cancer Res 50, 5558 5566.
31. Jaffrézou J-P, Levade T, Thurneyssen O, Chiron M, Bordier C, Attal M, Chatelain P Laurent G (1992) In vitro and in vivo enhancement of ricin-A chain immunotoxin activity by novel indolizine calcium channel blockers: delayed intracellular degradation linked to lipidosis induction. Cancer Res 52, 1352 1359.
32. Koishi R, Yoshimura C, Kohama T Serizawa N (2002) Leustroducsin B activates nuclear factor-κB via the acidic sphingomyelinase pathway in human bone marrow-derived stromal cell line KM-102. J Interferon Cytokine Res 22, 343 350.
33. Hurwitz R, Ferlinz K Sandhoff K (1994) The tricyclic antidepressant desipramine causes proteolytic degradation of lysosomal sphingomyelinase in human fibroblasts. Biol Chem Hoppe Seyler 375, 447 450.
34. Heinrich M, Wickel M, Schneider-Brachert W, Sandberg C, Gahr J, Schwandner R, Weber T, Saftig P, Peters C, Brunner J et al. (1999) Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J 18, 5252 5263.
35. Hundal RS, Gómez-Muñoz A, Kong JY, Salh BS, Marotta A, Duronio V Steinbrecher UP (2003) Oxidized low density lipoprotein inhibits macrophage apoptosis by blocking ceramide generation, thereby maintaining protein kinase B activation and Bcl-XL levels. J Biol Chem 278, 24399 24408.
36. Denys A, Aires V, Hichami A Khan NA (2004) Thapsigargin-stimulated MAP kinase phosphorylation via CRAC channels and PLD activation: inhibitory action of docosahexaenoic acid. FEBS Lett 564, 177 182.
37. Zeng L, An S Goetzl EJ (1996) Regulation of expression of matrix metalloproteinase-9 in early human T cells of the HSB.2 cultured line by the EP3 subtype of prostaglandin E2 receptor. J Biol Chem 271, 27744 27750.
38. Kato Y, Ozono S, Shuin T Miyazaki K (1996) Slow induction of gelatinase B mRNA by acidic culture conditions in mouse metastatic melanoma cells. Cell Biol Int 20, 375 377.
39. Williger BT, Ho WT Exton JH (1999) Phospholipase D mediates matrix metalloproteinase-9 secretion in phorbol ester-stimulated human fibrosarcoma cells. J Biol Chem 274, 735 738.
40. Rotin D, Robinson B Tannock IF (1986) Influence of hypoxia and an acidic environment on the metabolism and viability of cultured cells: potential implications for cell death in tumors. Cancer Res 46, 2821 2826.
41. Tannock IF Rotin D (1989) Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res 49, 4373 4384.
42. Yamagata M Tannock IF (1996) The chronic administration of drugs that inhibit the regulation of intracellular pH: in vitro and anti-tumour effects. Br J Cancer 73, 1328 1334.
43. Vukovic V Tannock IF (1997) Influence of low pH on cytotoxicity of paclitaxel, mitoxantrone and topotecan. Br J Cancer 75, 1167 1172.
44. Yamagata M, Hasuda K, Stamato T Tannock IF (1998) The contribution of lactic acid to acidification of tumours: studies of variant cells lacking lactate dehydrogenase. Br J Cancer 77, 1726 1731.
45. Griffiths L, Dachs GU, Bicknell R, Harris AL Stratford IJ (1997) 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 57, 570 572.
46. Bellocq A, Suberville S, Philippe C, Bertrand F, Perez J, Fouqueray B, Cherqui G Baud L (1998) 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 273, 5086 5092.
47. Shi Q, Le X, Wang B, Xiong Q, Abbruzzese JL Xie K (2000) Regulation of interleukin-8 expression by cellular pH in human pancreatic adenocarcinoma cells. J Interferon Cytokine Res 20, 1023 1028.
48. Xiong Q, Shi Q, Le X, Wang B Xie K (2001) Regulation of interleukin-8 expression by nitric oxide in human pancreatic adenocarcinoma. J Interferon Cytokine Res 21, 529 537.
49. 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.
50. Sato H Seiki M (1993) Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene 8, 395 405.
51. Lozano J, Berra E, Municio MM, Diaz-Meco MT, Dominguez I, Sanz L Moscat J (1994) Protein kinase C ζ isoform is critical for κB-dependent promoter activation by sphingomyelinase. J Biol Chem 269, 19200 19202.
52. Müller G, Ayoub M, Storz P, Rennecke J, Fabbro D Pfizenmaier K (1995) PKC ζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid. EMBO J 14, 1961 1969.
53. Duran A, Diaz-Meco MT Moscat J (2003) Essential role of RelA Ser311 phosphorylation by zetaPKC in NF-kappaB transcriptional activation. EMBO J 22, 3910 3918.
54. Akakura N, Kobayashi M, Horiuchi I, Suzuki A, Wang J, Chen J, Niizeki H, Kawamura K, Hosokawa M Asaka M (2001) Constitutive expression of hypoxia-inducible factor-1α renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res 61, 6548 6554.
55. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P et al. (1998) Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394, 485 490.
56. Helmlinger G, Sckell A, Dellian M, Forbes NS Jain RK (2002) Acid production in glycolysis-impaired tumors provides new insights into tumor metabolism. Clin Cancer Res 8, 1284 1291.
57. Estève PO, Chicoine È, Robledo O, Aoudjit F, Descoteaux A, Potworowski EF St-Pierre Y (2002) Protein kinase C-ζ regulates transcription of the matrix metalloproteinase-9 gene induced by IL-1 and TNF-α in glioma cells via NF-κB. J Biol Chem 277, 35150 35155.
58. Kato Y, Lewalle JM, Baba Y, Tsukuda M, Sakai N, Baba M, Kobayashi K, Koshika S, Nagashima Y, Frankenne F et al. (2001) Induction of SPARC by VEGF in human vascular endothelial cells. Biochem Biophys Res Commun 287, 422 426.
59. Labarca C Paigen K (1980) A simple, rapid, and sensitive DNA assay procedure. Anal Biochem 102, 344 352.
60. Kato Y, Nagashima Y, Koshikawa N, Miyagi Y, Yasumitsu H Miyazaki K (1998) Production of trypsins by human gastric cancer cells correlates with their malignant phenotype. Eur J Cancer 34, 1117 1123.
61. Baba Y, Tsukuda M, Mochimatsu I, Furukawa S, Kagata H, Nagashima Y, Sakai N, Koshika S, Imoto M et al. (2000) Inostamycin, an inhibitor of cytidine 5′-diphosphate 1,2-diacyl-sn-glycerol (CDP-DG): inositol transferase, suppresses invasion ability by reducing productions of matrix metalloproteinase-2 and -9 and cell motility in HSC-4 tongue carcinoma cell line. Clin Exp Metastasis 18, 273 279.
62. Liu G, Kleine L, Nasrallah R Hébert RL (1999) Bradykinin inhibits ceramide production and activates phospholipase D in rabbit cortical collecting duct cells. Am J Physiol 276, F589 F598.
63. Perry DK, Carton J, Shah AK, Meredith F, Uhlinger DJ Hannun YA (2000) Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis. J Biol Chem 275, 9078 9084.
64. Baba Y, Kato Y, Mochimatsu I, Nagashima Y, Kurihara M, Kawano T, Taguchi T, Hata R Tsukuda M (2004) Inostamycin suppresses vascular endothelial growth factor-stimulated growth and migration of human umbilical vein endothelial cells. Clin Exp Metastasis 21, 419 425.