High calcium concentration in bones promotes bone metastasis in renal cell carcinomas expressing calcium-sensing receptor

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Joeckel, Elke ^a   Haber, Tobias ^a   Prawitt, Dirk ^a   Junker, Kerstin ^b,c   Hampel, Christian ^a   Thüroff, Joachim W ^a   Roos, Frederik C ^a,c   Brenner, Walburgis ^a,c  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

^c For the German Renal Cell Tumor Network   (Germany)

Author keywords

Bone metastasis; Calcium sensing receptor; Microenvironment; Renal cell carcinoma

Indexed keywords

BROXURIDINE; CALCIUM; CALCIUM SENSING RECEPTOR; CHEMOTAXIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOTRANSFERASE;

ARTICLE; BONE METASTASIS; CANCER PATIENT; CANCER SURGERY; CANCER TISSUE; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; KIDNEY CARCINOMA; NEPHRECTOMY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

BLOTTING, WESTERN; BONE AND BONES; BONE NEOPLASMS; CALCIUM; CARCINOMA, RENAL CELL; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; KIDNEY NEOPLASMS; RECEPTORS, CALCIUM-SENSING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84896721627     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-42     Document Type: Article

References (48)

1. Woodward E, Jagdev S, McParland L, Clark K, Gregory W, Newsham A, Rogerson S, Hayward K, Selby P, Brown J. Skeletal complications and survival in renal cancer patients with bone metastases. Bone 2011, 48:160-166. 10.1016/j.bone.2010.09.008, 20854942.
2. Zekri J, Ahmed N, Coleman RE, Hancock BW. The skeletal metastatic complications of renal cell carcinoma. Int J Oncol 2001, 19:379-382.
3. Roodman GD. Mechanisms of bone metastasis. N Engl J Med 2004, 350:1655-1664. 10.1056/NEJMra030831, 15084698.
4. Jung ST, Ghert MA, Harrelson JM, Scully SP. Treatment of osseous metastases in patients with renal cell carcinoma. Clin Orthop Relat Res 2003, 409:223-231.
5. Han KR, Pantuck AJ, Bui MTB, Shvarts O, Freitas DG, Zisman A, Leibovich BC, Dorey FJ, Gitlitz BJ, Figlin RA, Belldegrun AS. Number of metastastic sites rather than location dictates overall survival of patients with node-negative metastatic renal cell carcinoma. Urology 2003, 61:314-319. 10.1016/S0090-4295(02)02163-5, 12597937.
6. Oppenheimer SB. Cellular basis of cancer metastasis: a review of fundamentals and new advances. Acta histochemica 2006, 108:327-334. 10.1016/j.acthis.2006.03.008, 16730054.
7. Woodhouse EC, Chuaqui RF, Liotta LA. General mechanisms of metastasis. Cancer 1997, 80:1529-1537. 10.1002/(SICI)1097-0142(19971015)80:8+<1529::AID-CNCR2>3.0.CO;2-F, 9362419.
8. Fidler IJ. Seed and soil revisited: contribution of the organ microenvironment to cancer metastasis. Surg Oncol Clin N Am 2001, 10:257-269.
9. Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 2009, 9:274-284. 10.1038/nrc2622, 19308067.
10. Chiang AC, Massagué J. Molecular basis of metastasis. N Engl J Med 2008, 359:2814-2823. 10.1056/NEJMra0805239, 19109576.
11. Mundy GR. Mechanisms of bone metastasis. Cancer Suppl 1997, 80:1546-1556.
12. Brown EM, Gamba G, Riccardi D, Lombardi M, Butters R, Kifor O, Sun A, Hediger MA, Lytton J, Hebert SC. Cloning and characterization of an extracellular Ca(2+)-sensing receptor from bovine parathyroid. Nature 1993, 366:575-580. 10.1038/366575a0, 8255296.
13. Diez-Fraile A, Lammens T, Benoit Y, D'Herde KG. The calcium-sensing receptor as a regulator of cellular fate in normal and pathological conditions. Curr Mol Med 2013, 13:282-295. 10.2174/156652413804810763, 23228129.
14. Riccardi D, Brown EM. Physiology and pathophysiology of the calcium-sensing receptor in the kidney. Am J Physiol Renal Physiol 2010, 298:F485-F499. 10.1152/ajprenal.00608.2009, 2838589, 19923405.
15. Ward DT, Riccardi D. New concepts in calcium-sensing receptor pharmacology and signalling. Br J Pharmacol 2012, 165:35-48. 10.1111/j.1476-5381.2011.01511.x, 3252964, 21627634.
16. Atchison DK, Beierwaltes WH. The influence of extracellular and intracellular calcium on the secretion of renin. Pflugers Arch 2013, 465:59-69. 10.1007/s00424-012-1107-x, 3553253, 22538344.
17. Brennan SC, Connigrave AD. Regulation of cellular signal transduction pathways by the extracellular calcium-sensing receptor. Curr Pharm Biotechnol 2009, 10:270-281. 10.2174/138920109787847484, 19355937.
18. Mihai R, Stevens J, McKinney C, Ibrahim NB. Expression of the calcium receptor in human breast cancer - a potential new marker predicting the risk of bone metastases. Eur J Surg Oncol 2006, 32:511-515. 10.1016/j.ejso.2006.02.009, 16564154.
19. Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 1989, 8:98-101.
20. Boyce BF. Bone biology and pathology. Handbook of Cancer-Related Bone Disease 2012, 3-21. Bristol, UK: Published by BioScientifica Ltd, 2.
21. Peacock M. Hypercalcaemia and calcium homeostasis. Metab Bone Dis & Rel Res 1980, 2:143-150.
22. Cheng I, Klingensmith ME, Chattopadhyay N, Kifor O, Butters RR, Soybel DI, Brown EM. Identification and localization of the extracellular calcium-sensing receptor in human breast. J Clin Endocrinol Metab 1998, 83:703-707.
23. Mihai R. The calcium sensing receptor: from understanding parathyroid calcium homeostasis to bone metastases. Ann R Coll Surg Engl 2008, 90:271-277. 10.1308/003588408X286044, 2647185, 18492387.
24. Saidak Z, Mentaverri R, Brown EM. The role of the calcium-sensing receptor in the development and progression of cancer. Endocr Rev 2009, 30:178-195. 10.1210/er.2008-0041, 19237714.
25. Rogers KV, Dunn CK, Conklin RL, Hadfield S, Petty BA, Brown EM, Hebert SC, Nemeth EF, Fox J. Calcium receptor messenger ribonucleic acid levels in the parathyroid glands and kidney of vitamin D-deficient rats are not regulated by plasma calcium or 1,25-dihydroxyvitamin D3. Endocrinology 1995, 136:499-504.
26. Saidak Z, Boudot C, Abdoune R, Petit L, Brazier M, Mentaverri R, Kamel S. Extracellular calcium promotes the migration of breast cancer cells through the activation of the Calcium sensing receptor. Exp Cell Res 2072-2080, 2009:315.
27. Liao J, Schneider A, Datta NS, McCauley LK. Extracellular calcium as a candidate mediator of prostate cancer skeletal metastasis. Cancer Res 2006, 66:9065-9073. 10.1158/0008-5472.CAN-06-0317, 16982748.
28. Manning AT, O'Brien N, Kerin MJ. Roles for the calcium sensing receptor in primary and metastatic cancer. EJSO 2006, 32:693-697. 10.1016/j.ejso.2006.03.047, 16765016.
29. Chattopadhyay N, Ye CP, Yamaguchi T, Kerner R, Vassilev PM, Brown EM. Extracellular calcium-sensing receptor induces cellular proliferation and activation of a nonselective cation channel in U373 human astrocytoma cells. Brain Res 1999, 851:116-124. 10.1016/S0006-8993(99)02132-0, 10642834.
30. Hobson SA, McNeil SE, Lee F, Rodland KD. Signal transduction mechanisms linking increased extracellular calcium to proliferation in ovarian surface epithelial cells. Exp Cell Res 2000, 258:1-11. 10.1006/excr.2000.4910, 10912782.
31. Saxena H, Deshpande DA, Tiegs BC, Yan H, Battafarano RJ, Burrows WM, Damera G, Panettieri RA, Dubose TD, An SS, Penn RB. The GPCR OGR1 (GPR68) mediates diverse signalling and contraction of airway smooth muscle in response to small reductions in extracellular pH. Br J Pharmacol 2012, 166:981-990. 10.1111/j.1476-5381.2011.01807.x, 3417423, 22145625.
32. Rogers AC, Hanly AM, Collins D, Baird AW, Winter DC. Review article: loss of the calcium-sensing receptor in colonic epithelium is a key event in the pathogenesis of colon cancer. Clin Colorectal Cancer 2012, 11:24-30. 10.1016/j.clcc.2011.04.003, 21723793.
33. Casalà C, Gil-Guiñón E, Ordóñez JL, Miguel-Queralt S, Rodríguez E, Galván P, Lavarino C, Munell F, de Alava E, Mora J, de Torres C. The calcium-sensing receptor is silenced by genetic and epigenetic mechanisms in unfavorable neuroblastomas and its reactivation induces ERK1/2-dependent apoptosis. Carcinogenesis 2013, 34:268-276. 10.1093/carcin/bgs338, 23108190.
34. Huang C, Miller RT. The calcium-sensing receptor and its interacting proteins. J Cell Mol Med 2007, 11:923-934. 10.1111/j.1582-4934.2007.00114.x, 17979874.
35. Brown EM, MacLeod RJ. Extracellular calcium sensing and extracellular calcium signaling. Physiol Rev 2001, 81:239-297.
36. Li HX, Kong FJ, Bai SZ, He W, Xing WJ, Xi YH, Li GW, Guo J, Li HZ, Wu LY, Wang R, Yang GD, Tian Y, Xu CQ. Involvement of calcium-sensing receptor in oxLDL-induced MMP-2 production in vascular smooth muscle cells via PI3K/Akt pathway. Mol Cell Biochem 2012, 362:115-122. 10.1007/s11010-011-1133-6, 22083546.
37. Turner CE. Paxillin. Int J Biochem Cell Biol 1998, 30:955-959. 10.1016/S1357-2725(98)00062-4, 9785458.
38. Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K. JNK phosphorylates paxillin and regulates cell migration. Nature 2003, 424:219-223. 10.1038/nature01745, 12853963.
39. Tfelt-Hansen J, Chattopadhyay N, Yando S, Kanuparthi D, Rooney P, Schwarz P, Brown EM. Calcium-sensing receptor induces proliferation through p38 mitogen-activated protein kinase and phosphatidylinositol 3-kinase but not extracellularly regulated kinase in a model of humoral hypercalcemia of malignancy. Endocrinology 2004, 145:1211-1217. 10.1210/en.2003-0749, 14645111.
40. Tfelt-Hansen J, MacLeod RJ, Chattopadhyay N, Yano S, Quinn S, Ren X, Terwilliger EF, Schwarz P, Brown EM. Calcium-sensing receptor stimulates PTHrP release by pathways dependent on PKC, p38 MAPK, JNK, and ERK1/2 in H-500 cells. Am J Physiol Endocrinol Metab 2003, 285:E329-E337.
41. Davey AE, Leach K, Valant C, Conigrave AD, Sexton PM, Christopoulos A. Positive and negative allosteric modulators promote biased signaling at the calcium-sensing receptor. Endocrinology 2012, 153:1232-1241. 10.1210/en.2011-1426, 22210744.
42. Chakravarti B, Dwivedi SK, Mithal A, Chattopadhyay N. Calcium-sensing receptor in cancer: good cop or bad cop?. Endocr 2009, 35:271-284.
43. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998, 273:13375-13378. 10.1074/jbc.273.22.13375, 9593664.
44. Kölsch V, Charest PG, Firtel RA. The regulation of cell motility and chemotaxis by phospholipid signaling. J Cell Sci 2008, 121:551-559. 10.1242/jcs.023333, 2671295, 18287584.
45. Yamada KM, Araki M. Tumor suppressor PTEN: modulator of cell signaling, growth, migration and apoptosis. J of Cell Sci 2001, 114:2375-2382.
46. Schneider E, Keppler R, Prawitt D, Steinwender C, Roos FC, Thüroff JW, Lausch E, Brenner W. Migration of renal tumor cells depends on dephosphorylation of Shc by PTEN. Int J Oncol 2011, 38:823-831.
47. Brenner W, Greber I, Gudejko-Thiel J, Beitz S, Schneider E, Walenta S, Peters K, Unger R, Thüroff JW. Migration of renal carcinoma cells is dependent on protein kinase Cdelta via beta1 integrin and focal adhesion kinase. Int J Oncol 2008, 32:1125-1131.
48. Brenner W, Beitz S, Schneider E, Benzing F, Unger RE, Roos FC, Thüroff JW, Hampel C. Adhesion of renal carcinoma cells to endothelial cells depends on PKCμ. BMC Cancer 2010, 10:183. 10.1186/1471-2407-10-183, 2873397, 20459627.