Bradykinin-induced $Ca^{2+}$ signaling in human oral squamous cell carcinoma HSC-3 cells

  • Sohn, Byung-Jin (Department of Physiology and Dental Research Institute, Seoul National University School of Dentistry) ;
  • Kang, Ji-Ah (Department of Physiology and Dental Research Institute, Seoul National University School of Dentistry) ;
  • Jo, Su-Hyun (Department of Physiology, Kangwon National University School of Medicine) ;
  • Choi, Se-Young (Department of Physiology and Dental Research Institute, Seoul National University School of Dentistry)
  • Published : 2009.06.30

Abstract

Cytosolic $Ca^{2+}$ is an important regulator of tumor cell proliferation and metastasis. Recently, the strategy of blocking receptors and channels specific to certain cancer cell types has emerged as a potentially viable future treatment. Oral squamous cell carcinoma is an aggressive form of cancer with a high metastasis rate but the receptor-mechanisms involved in $Ca^{2+}$ signaling in these tumors have not yet been elucidated. In our present study, we report that bradykinin induces $Ca^{2+}$ signaling and its modulation in the human oral squamous carcinoma cell line, HSC-3. Bradykinin was found to increase the cytosolic $Ca^{2+}$ levels in a concentration-dependent manner. This increase was inhibited by pretreatment with the phospholipase C-${\beta}$ inhibitor, U73122, and also by 2-aminoethoxydiphenyl borate, an inhibitor of the inositol 1,4,5-trisphosphate receptor. Pretreatment with extracellular ATP also inhibited the peak bradykinin-induced $Ca^{2+}$ rise. In contrast, the ATP-induced rise in cytosolic $Ca^{2+}$ was not affected by pretreatment with bradykinin. Pretreatment of the cells with either forskolin or phorbol 12-myristate 13-acetate (activators of adenylyl cyclase and protein kinase C, respectively) prior to bradykinin application accelerated the recovery of cytosolic $Ca^{2+}$ to baseline levels. These data suggest that bradykinin receptors are functional in $Ca^{2+}$ signaling in HSC-3 cells and may therefore represent a future target in treatment strategies for human oral squamous cell carcinoma.

References

  1. Barki-Harrington L, Bookout AL, Wang G, Lamb ME, Leeb-Lundberg LM, Daaka Y. Requirement for direct cross-talk between B1 and B2 kinin receptors for the proliferation of androgen-insensitive prostate cancer PC3 cells. Biochem J. 2003;371:581-7 https://doi.org/10.1042/BJ20021708
  2. Bhoola KD, Figueroa CD, Worthy K. Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol Rev. 1992;44:1-80
  3. Chan DC, Gera L, Stewart JM, Helfrich B, Zhao TL, Feng WY, Chan KK, Covey JM, Bunn PA Jr. Bradykinin antagonist dimer, CU201, inhibits the growth of human lung cancer cell lines in vitro and in vivo and produces synergistic growth inhibition in combination with other antitumor agents. Clin Cancer Res. 2002;8:1280-7
  4. Choi SY, Choi BH, Suh BC, Chae HD, Kim JS, Shin MJ, Kang SS, Negishi M, Kim KT. Potentiation of PGE2-mediated cAMP production during neuronal differentiation of human neuroblastoma SK-N-BE(2)C cells. J Neurochem. 2001;79:303-10 https://doi.org/10.1046/j.1471-4159.2001.00577.x
  5. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5) $P_{2}$-mediated inhibition. Nature 2001;411:957-62 https://doi.org/10.1038/35082088
  6. Endo Y, Uzawa K, Mochida Y, Shiiba M, Bukawa H, Yokoe H, Tanzawa H. Sarcoendoplasmic reticulum $Ca^{2+}$ ATPase type 2 downregulated in human oral squamous cell carcinoma. Int J Cancer. 2004;110:225-31 https://doi.org/10.1002/ijc.20118
  7. Ferguson PJ, Currie C, Vincent MD. Enhancement of platinumdrug cytotoxicity in a human head and neck squamous cell carcinoma line and its platinum-resistant variant by liposomal amphotericin B and phospholipase A2-II. Drug Metab Dispos. 1999;27:1399-405
  8. Grynkiewicz G, Poenie M, Tsien RY. A new generation of $Ca^{2+}$ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260:3440-50
  9. Hosoi K, Kurihara K, Ueha T. Bradykinin-stimulated transient modulation of epidermal growth factor receptors in A-431 human epidermoid carcinoma cells. J Cell Physiol. 1993;157:1-12 https://doi.org/10.1002/jcp.1041570102
  10. Hsieh HL, Wu CY, Hwang TL, Yen MH, Parker P, Yang CM. BK-induced cytosolic phospholipase $A_{2}$ expression via sequential PKC-$\delta$, p42/p44 MAPK, and NF-$\kappa{B}$ activation in rat brain astrocytes. J Cell Physiol. 2006;206:246-54 https://doi.org/10.1002/jcp.20457
  11. Kato H, Uzawa K, Onda T, Kato Y, Saito K, Nakashima D, Ogawara K, Bukawa H, Yokoe H, Tanzawa H. Downregulation of 1D-myo-inositol 1,4,5-trisphosphate 3-kinase A protein expression in oral squamous cell carcinoma. Int J Oncol. 2006b;28:873-81
  12. Kato Y, Uzawa K, Saito K, Nakashima D, Kato M, Nimura Y, Seki N, Tanzawa H. Gene expression pattern in oral cancer cervical lymph node metastasis. Oncol Rep. 2006a;16:1009-14
  13. Kokoska ER, Wolff AB, Smith GS, Miller TA. Epidermal growth factor-induced cytoprotection in human intestinal cells involves intracellular calcium signaling. J Surg Res. 2000;88:97-103 https://doi.org/10.1006/jsre.1999.5740
  14. Kurahara S, Shinohara M, Ikebe T, Nakamura S, Beppu M, Hiraki A, Takeuchi H, Shirasuna K. Expression of MMPS, MT-MMP, and TIMPs in squamous cell carcinoma of the oral cavity: correlations with tumor invasion and metastasis. Head Neck. 1999;21:627-38 https://doi.org/10.1002/(SICI)1097-0347(199910)21:7<627::AID-HED7>3.0.CO;2-2
  15. Lai J, Luo MC, Chen Q, Ma S, Gardell LR, Ossipov MH, Porreca F. Dynorphin A activates bradykinin receptors to maintain neuropathic pain. Nat Neurosci. 2006;9:1534-40 https://doi.org/10.1038/nn1804
  16. Lee WJ, Roberts-Thomson SJ, Holman NA, May FJ, Lehrbach GM, Monteith GR. Expression of plasma membrane calcium pump isoform mRNAs in breast cancer cell lines. Cell Signal. 2002;14:1015-22 https://doi.org/10.1016/S0898-6568(02)00049-9
  17. Liu LH, Boivin GP, Prasad V, Periasamy M, Shull GE. Squamous cell tumors in mice heterozygous for a null allele of Atp2a2, encoding the sarco(endo)plasmic reticulum $Ca^{2+}$-ATPase isoform 2 $Ca^{2+}$ pump. J Biol Chem. 2001;276:26737-40 https://doi.org/10.1074/jbc.C100275200
  18. Lumenta DB, Plesnila N, Kläsner B, Baethmann A, Pruneau D, Schmid-Elsaesser R, Zausinger S. Neuroprotective effects of a postischemic treatment with a bradykinin $B_{2}$https://doi.org/10.1016/j.brainres.2005.11.043
  19. Mahabeer R, Bhoola KD. Kallikrein and kinin receptor genes. Pharmacol Ther. 2000;88:77-89 https://doi.org/10.1016/S0163-7258(00)00080-2
  20. Min JH, Kim DK, Lee MH, Bae MK, Um KI, Kwak HH, Park BS, Kim GC. Mutantional analysis of tumor suppressor gene p53 in human oral squmous carcinoma cell line YD-9. Int J Oral Biol. 2007;32:79-84
  21. Momose F, Araida T, Negishi A, Ichijo H, Shioda S, Sasaki S. Variant sublines with different metastatic potentials selected in nude mice from human oral squamous cell carcinomas. J Oral Pathol Med. 1989;18:391-5 https://doi.org/10.1111/j.1600-0714.1989.tb01570.x
  22. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ. Calcium and cancer: targeting $Ca^{2+}$ transport. Nat Rev Cancer. 2007;7:519-30 https://doi.org/10.1038/nrc2171
  23. Myoung H, Hong SP, Yun PY, Lee JH, Kim MJ. Anti-cancer effect of genistein in oral squamous cell carcinoma with respect to angiogenesis and in vitro invasion. Cancer Sci. 2003;94:215-20 https://doi.org/10.1111/j.1349-7006.2003.tb01422.x
  24. Ongali B, Campos MM, Bregola G, Rodi D, Regoli D, Thibault G, Simonato M, Couture R. Autoradiographic analysis of rat brain kinin $B_{1}$ and $B_{2}$ receptors: normal distribution and alterations induced by epilepsy. J Comp Neurol. 2003;461:506-19 https://doi.org/10.1002/cne.10706
  25. Parkin DM, Pisani P, Ferlay J. Global cancer statistics. CA Cancer J Clin. 1999;49:33-64 https://doi.org/10.3322/canjclin.49.1.33
  26. Prasad V, Boivin GP, Miller ML, Liu LH, Erwin CR, Warner BW, Shull GE. Haploinsufficiency of Atp2a2, encoding the sarco(endo)plasmic reticulum $Ca^{2+}$-ATPase isoform 2 $Ca^{2+}$ pump, predisposes mice to squamous cell tumors via a novel mode of cancer susceptibility. Cancer Res. 2005;65:8655-61 https://doi.org/10.1158/0008-5472.CAN-05-0026
  27. Raidoo DM, Sawant S, Mahabeer R, Bhoola KD. Kinin receptors are expressed in human astrocytic tumour cells. Immunopharmacology. 1999;43:255-63 https://doi.org/10.1016/S0162-3109(99)00097-1
  28. Roderick HL, Cook SJ. $Ca^{2+}$ signalling checkpoints in cancer: remodelling $Ca^{2+}$ for cancer cell proliferation and survival. Nat Rev Cancer. 2008;8:361-75 https://doi.org/10.1038/nrc2374
  29. Roy SS, Madesh M, Davies E, Antonsson B, Danial N, Hajn$\acute{o}$czky G. Bad targets the permeability transition pore independent of Bax or Bak to switch between $Ca^{2+}$-dependent cell survival and death. Mol Cell. 2009;33:377-88 https://doi.org/10.1016/j.molcel.2009.01.018
  30. Saito K, Uzawa K, Endo Y, Kato Y, Nakashima D, Ogawara K, Shiba M, Bukawa H, Yokoe H, Tanzawa H. Plasma membrane $Ca^{2+}$ ATPase isoform 1 down-regulated in human oral cancer. Oncol Rep. 2006;15:49-55
  31. Shen X, Kramer RH.Adhesion-mediated squamous cell carcinoma survival through ligand-independent activation of epidermal growth factor receptor. Am J Pathol. 2004;165:1315-29
  32. Son HJ, Chu JY, Cho ES, Lee DG, Min MG, Lee SK, Cho NP. Methylation status and expression of E-cadherin in oral squamous cell carcinomas compared to benighn oral epithelial lesions. Int J Oral Biol. 2006;31:27-32
  33. Stewart JM, Gera L, Chan DC, Bunn PA Jr, York EJ, Simkeviciene V, Helfrich B. Bradykinin-related compounds as new drugs for cancer and inflammation. Can J Physiol Pharmacol. 2002;80:275-80 https://doi.org/10.1139/y02-030
  34. Stewart JM, Gera L, Chan DC, York EJ, Simkeviciene V, Bunn PA Jr, Taraseviciene-Stewart L. Combination cancer chemotherapy with one compound: pluripotent bradykinin antagonists. Peptides. 2005;26:1288-91 https://doi.org/10.1016/j.peptides.2005.03.052
  35. Taub JS, Guo R, Leeb-Lundberg LM, Madden JF, Daaka Y. Bradykinin receptor subtype 1 expression and function in prostate cancer. Cancer Res. 2003;63:2037-41
  36. Taylor JT, Huang L, Pottle JE, Liu K, Yang Y, Zeng X, Keyser BM, Agrawal KC, Hansen JB, Li M. Selective blockade of T-type $Ca^{2+}$ channels suppresses human breast cancer cell proliferation. Cancer Lett. 2008;267:116-24 https://doi.org/10.1016/j.canlet.2008.03.032
  37. Thomas SM, Coppelli FM, Wells A, Gooding WE, Song J, Kassis J, Drenning SD, Grandis JR. Epidermal growth factor receptor-stimulated activation of phospholipase Cgamma-1 promotes invasion of head and neck squamous cell carcinoma. Cancer Res. 2003;63:5629-35
  38. Tsujimoto Y, Nakagawa T, Shimizu S. Mitochondrial membrane permeability transition and cell death. Biochim Biophys Acta. 2006;1757:1297-300 https://doi.org/10.1016/j.bbabio.2006.03.017
  39. Usachev YM, Toutenhoofd SL, Goellner GM, Strehler EE, Thayer SA. Differentiation induces up-regulation of plasma membrane $Ca^{2+}$-ATPase and concomitant increase in $Ca^{2+}$ efflux in human neuroblastoma cell line IMR-32. J Neurochem. 2001;76:1756-65 https://doi.org/10.1046/j.1471-4159.2001.00169.x
  40. Wang SJ, Bourguignon LY. Hyaluronan and the interaction between CD44 and epidermal growth factor receptor in oncogenic signaling and chemotherapy resistance in head and neck cancer. Arch Otolaryngol Head Neck Surg. 2006;132:771-8 https://doi.org/10.1001/archotol.132.7.771
  41. Wang H, Kohno T, Amaya F, Brenner GJ, Ito N, Allchorne A, Ji RR, Woolf CJ. Bradykinin produces pain hypersensitivity by potentiating spinal cord glutamatergic synaptic transmission. J Neurosci. 2005;25:7986-92 https://doi.org/10.1523/JNEUROSCI.2393-05.2005
  42. Werry TD, Wilkinson GF, Willars GB. Mechanisms of crosstalk between G-protein-coupled receptors resulting in enhanced release of intracellular $Ca^{2+}$. Biochem J. 2003;374:281-96 https://doi.org/10.1042/BJ20030312
  43. Wu J, Akaike T, Maeda H. Modulation of enhanced vascular permeability in tumors by a bradykinin antagonist, a cyclooxygenase inhibitor, and a nitric oxide scavenger. Cancer Res. 1998;58:159-65