Review article: Loss of the calcium-sensing receptor in colonic epithelium is a key event in the pathogenesis of colon cancer

Clinical Colorectal Cancer

Volumn 11, Issue 1, 2012, Pages 24-30

  Rogers, Ailín C ^a,b   Hanly, Ann M ^a   Collins, Danielle ^a,b   Baird, Alan W ^b   Winter, Desmond C ^a  

^a ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Calcium homeostasis; Cell proliferation; Vitamin D

Indexed keywords

ACTIN; ADENYLATE CYCLASE; APC PROTEIN; BETA CATENIN; CALCIMIMETIC AGENT; CALCIUM; CALCIUM ION; CALCIUM SENSING RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; SPERMINE; SURVIVIN; T CELL FACTOR PROTEIN; UVOMORULIN; VITAMIN D;

CALCIUM CELL LEVEL; CALCIUM INTAKE; CALCIUM SIGNALING; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CANCER STAGING; CELL CYCLE; CELL DIFFERENTIATION; CELL JUNCTION; CELL PROLIFERATION; COLON ADENOMA; COLON CANCER; COLON CARCINOGENESIS; COLON MUCOSA; COMPLEX FORMATION; CRYPT CELL; CYTOSOL; DISEASE PREDISPOSITION; EPITHELIUM CELL; HUMAN; PATHOGENESIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR BINDING; REVIEW; TUMOR DIFFERENTIATION;

EID: 84861534670     PISSN: 15330028     EISSN: 19380674     Source Type: Journal    
DOI: 10.1016/j.clcc.2011.04.003     Document Type: Review

References (64)

1. Garland C, Shekelle RB, Barrett-Connor E, et al. Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men. Lancet 1985; 1:307-9.
2. Sellers TA, Bazyk AE, Bostick RM, et al. Diet and risk of colon cancer in a large prospective study of older women: an analysis stratified on family history. Cancer Causes Control 1998; 9:357-67.
3. Wu K, Willett WC, Fuchs CS, et al. Calcium intake and risk of colon cancer in women and men. J Natl Cancer Inst 2002; 94:437-46.
4. Baron JA, Beach M, Mandel JS, et al. Calcium supplements for the prevention of colorectal adenomas. Calcium Polyp Prevention Study Group. N Engl J Med 1999; 340:101-7.
5. Bonithon-Kopp C, Kronborg O, Giacosa A, et al. Calcium and fibre supplementation in prevention of colorectal adenoma recurrence: a randomised intervention trial. European Cancer Prevention Organisation Study Group. Lancet 2000; 356: 1300-6.
6. Wargovich MJ, Jimenez A, McKee K, et al. Efficacy of potential chemopreventive agents on rat colon aberrant crypt formation and progression. Carcinogenesis 2000; 21:1149-55.
7. Penman ID, Liang QL, Bode J, et al. Dietary calcium supplementation increases apoptosis in the distal murine colonic epithelium. J Clin Pathol 2000; 53:302-7.
8. Ahearn TU, McCullough ML, Flanders WD, et al. A randomized clinical trial of the effects of supplemental calcium and vitamin D3 on markers of their metabolism in normal mucosa of colorectal adenoma patients. Cancer Res 2011; 71: 413-23.
9. Brown EM, Gamba G, Riccardi D, et al. Cloning, expression, and characterization of an extracellular Ca2+ sensing receptor from bovine parathyroid. Nature 1993; 366:575-80.
10. Brown EM, MacLeod RJ. Extracellular calcium sensing and extracellular calcium signaling. Physiol Rev 2001; 81:239-97.
11. Chang W, Shoback D. Extracellular Ca2+-sensing receptors-an overview. Cell Calcium 2004; 35:183-96.
12. Gama L, Baxendale-Cox LM, Breitwieser GE. Ca2+-sensing receptors in intestinal epithelium. Am J Physiol 1997; 273:C1168-75.
13. Kállay E, Bonner E, Wrba F, et al. Molecular and functional characterization of the extracellular calcium-sensing receptor in human colon cancer cells. Oncol Res 2003; 13:551-9.
14. Sheinin Y, Kállay E, Wrba F, et al. Immunocytochemical localization of the extracellular calcium-sensing receptor in normal and malignant human large intestinal mucosa. J Histochem Cytochem 2000; 48:595-602.
15. Bostick RM, Fosdick L, Wood JR. Calcium and colorectal epithelial cell proliferation in sporadic adenoma patients: a randomized, double-blinded, placebo controlled clinical trial. J Natl Cancer Inst 1995; 87:1307-15.
16. Baron JA, Beach M. A randomized trial of calcium supplementation to prevent colorectal adenomas. Gastroenterology 1998; 114:A563.
17. Holt PR, Atillasoy EO, Gilman J, et al. Modulation of abnormal colonic epithelial cell proliferation and differentiation by low-fat dairy foods: a randomized controlled trial. JAMA 1998; 280:1074-9.
18. Lipkin M. Early development of cancer chemoprevention clinical trials: studies of dietary calcium as a chemopreventive agent for human subjects. Eur J Cancer Prev 2002; 11:S65-70.
19. Manning AT, O'Brien N, Kerin MJ. Roles for the calcium sensing receptor in primary and metastatic cancer. Eur J Surg Oncol 2006; 32:693-7.
20. Justinich CJ, Mak N, Pacheco I, et al. The extracellular calcium-sensing receptor (CaSR) on human esophagus and evidence of expression of the CaSR on the esophageal epithelial cell line (HET-1A). Am J Physiol Gastrointest Liver Physiol 2008; 294:G120-9.
21. Dufner MM, Kirchhoff P, Remy C, et al. The calcium-sensing receptor acts as a modulator of gastric acid secretion in freshly isolated human gastric glands. Am J Physiol Gastrointest Liver Physiol 2005; 289:G1084-90.
22. Chattopadhyay N, Cheng I, Rogers K, et al. Identification and localization of extracellular Ca(2+)-sensing receptor in rat intestine. Am J Physiol 1998; 274: G122-30.
23. Chakrabarty S, Wang H, Canaff L, et al. Calcium sensing receptor in human colon carcinoma: interaction with Ca2+ and 1,25-dihydroxyvitamin D3. Cancer Res 2005; 65:493-8.
24. Buras RR, Shabahang M, Davoodi F, et al. The effect of extracellular calcium on colonocytes: evidence for differential responsiveness based upon degree of cell differentiation. Cell Prolif 1995; 28:245-62.
25. Whitfield JF, Bird RP, Chakravarthy BR, et al. Calcium-cell cycle regulator, differentiator, killer, chemopreventor, and maybe, tumor promoter. J Cell Biochem Suppl 1995; 22:74-91.
26. Brenner BM, Russell N, Albrecht S, et al. The effect of dietary vitamin D3 on the intracellular calcium gradient in mammalian colonic crypts. Cancer Lett 1998; 127: 43-53.
27. Cheng SX, Geibel JP, Hebert SC. Extracellular polyamines regulate fluid secretion in rat colonic crypts via the extracellular calcium-sensing receptor. Gastroenterology 2004; 126:148-58.
28. Huang C, Miller RT. The calcium-sensing receptor and its interacting proteins. J Cell Mol Med 2007; 11:923-34.
29. Quinn SJ, Ye CP, Diaz R, et al. The Ca2+-sensing receptor: a target for polyamines. Am J Physiol Cell Physiol 1997; 273:1315-23.
30. Liu G, Hu X, Premkumar L, et al. Nifedipine synergizes with calcium in activating the calcium sensing receptor, suppressing the expression of thymidylate synthase and survivin and promoting sensitivity to fluorouracil in human colon carcinoma cells. Mol Carcinog 2011 [Epub ahead of print].
31. Bai M. Structure-function relationship of the extracellular calcium-sensing receptor. Cell Calcium 2004; 35:197-207.
32. Brown EM, Enyedi P, LeBoff M, et al. High extracellular Ca 2+ and Mg 2+ stimulate accumulation of inositol phosphates in bovine parathyroid cells. FEBS Lett 1987; 218:113-8.
33. Miedlich S, Gama L, Breitwieser GE. Calcium sensing receptor activation by a calcimimetic suggests a link between cooperativity and intracellular calcium oscillations. J Biol Chem 2002; 277:49691-9.
34. Young SH, Rozengurt E. Amino acids and Ca2+ stimulate different patterns of Ca2+ oscillations through the Ca 2+-sensing receptor. Am J Physiol Cell Physiol 2002; 282:C1414-22.
35. Rey O, Young SH, Jacamo R, et al. Extracellular calcium sensing receptor stimulation in human colonic epithelial cells induces intracellular calcium oscillations and proliferation inhibition. J Cell Physiol 2010; 225:73-83.
36. Dolmetsch RE, Xu K, Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998; 392:933-6.
37. Li W, Llopis J, Whitney M, et al. Cell-permeant caged InsP3 ester shows that calcium spike frequency can optimize gene expression. Nature 1998; 392:936-41.
38. Bhagavathula N, Kelley EA, Reddy M, et al. Upregulation of calcium-sensing receptor and mitogen-activated protein kinase signalling in the regulation of growth and differentiation in colon carcinoma. Br J Cancer 2005; 93:1364-71.
39. Taupin D, Podolsky DK. Mitogen-activated protein kinase activation regulates intestinal epithelial differentiation. Gastroenterology 1999; 116:1072-80.
40. Corbetta S, Eller-Vainicher C, Vicentini L, et al. Modulation of cyclin D1 expression in human tumoral parathyroid cells: effects of growth factors and calcium sensing receptor activation. Cancer Lett 2007; 255:34-41.
41. Lin KI, Chattopadhyay N, Bai M, et al. Elevated extracellular calcium can prevent apoptosis via the calcium-sensing receptor. Biochem Biophys Res Commun 1998; 249:325-31.
42. Birchmeier W. E-cadherin as a tumor (invasion) suppressor gene. Bioessays 1995; 17:97-9.
43. Mareel M, Berx G, Van Roy F, et al. Cadherin/catenin complex: a target for antiinvasive therapy? J Cell Biochem 1996; 61:524-30.
44. Bhagavathula N, Hanosh AW, Nerusu KC, et al. Regulation of E- cadherin and beta-catenin by calcium in colon carcinoma is dependent on calcium-sensing receptor expression and function. Int J Cancer 2007; 121:1455-62.
45. Brattain MG, Brattain DE, Fine WD, et al. Initiation of cultures of human colonic carcinoma with different biological characteristics utilizing feeder layers of confluent fibroblasts. Oncodev Biol Med 1981; 2:355-66.
46. Saidak Z, Mentaverri R, Brown EM. The role of the calcium-sensing receptor in the development and progression of cancer. Endocr Rev 2010; 30:178-95.
47. Cheng I, Klingensmith M, Chattopadhyay N, et al. Identification and localization of the extracellular calcium-sensing receptor in human breast. J Clin Endocrinol Metab 1998; 83:703-7.
48. McNeil L, Hobson S, Nipper V, et al. Functional calcium-sensing receptor expression in ovarian surface epithelial cells. Am J Obstet Gynecol 1998; 178:305-13.
49. Tu CL, Oda Y, Komuves L, et al. The role of the calcium-sensing receptor in epidermal differentiation. Cell Calcium 2004; 35:265-73.
50. McGrath C, Soule H. Calcium regulation of normal human mammary epithelial cell growth in culture. In Vitro Cell Dev Biol 1984; 20:652-62.
51. Ochieng J, Tahin Q, Booth C, et al. Buffering of intracellular calcium in response to increased extracellular levels in mortal, immortal, and transformed human breast epithelial cells. J Cell Biochem 1991; 46:250-4.
52. Liu G, Hu X, Chakrabarty S. Calcium sensing receptor down-regulates malignant cell behavior and promotes chemosensitivity in human breast cancer cells. Cell Calcium 2009; 45:216-25.
53. Hobson SA, McNeil SE, Lee F, et al. Signal transduction mechanisms linking increased extracellular calcium to proliferation in ovarian surface epithelial cells. Exp Cell Res 2000; 258:1-11.
54. Buset M, Lipkin M, Winawer S, et al. Inhibition of human colonic epithelial cell proliferation in vivo and in vitro by calcium. Cancer Res 1986; 46:5426-30.
55. Whitfield JF. Calcium, calcium-sensing receptor and colon cancer. Cancer Lett 2009; 275:9-16.
56. Hizaki K, Yamamoto H, Taniguchi H, et al. Epigenetic inactivation of calciumsensing receptor in colorectal carcinogenesis. Mod Pathol 2011 [Epub ahead of print].
57. Jenab M, McKay J, Bueno-de-Mesquita HB, et al. Vitamin D receptor and calcium sensing receptor polymorphisms and the risk of colorectal cancer in European populations. Cancer Epidemiol Biomarkers Prev 2009; 18:2485-91.
58. Jacobs ET, Martínez ME, Campbell PT, et al. Genetic variation in the retinoid X receptor and calcium-sensing receptor and risk of colorectal cancer in the Colon Cancer Family Registry. Carcinogenesis 2010; 31:1412-6.
59. Pitari GM, Lin JE, Shah FJ, et al. Enterotoxin preconditioning restores calcium-sensing receptor mediated cytostasis in colon cancer cells. Carcinogenesis 2008; 29:1601-7.
60. Liu G, Hu X, Varani J, et al. Calcium and calcium sensing receptor modulates the expression of thymidylate synthase, NAD(P)H:quinone oxidoreductase 1 and survivin in human colon carcinoma cells: promotion of cytotoxic response to mitomycin C and fluorouracil. Mol Carcinog 2009; 48:202-11.
61. Wang X, Chen W, Singh N, et al. Effects of potential calcium sensing receptor inducers on promoting chemosensitivity of human colon carcinoma cells. Int J Oncol 2010; 36:1573-80.
62. Shabahang M, Buras RR, Davoodi F, et al. 1,25-Dihydroxyvitamin D3 receptor as a marker of human colon carcinoma cell line differentiation and growth inhibition. Cancer Res 1993; 53:3712-8.
63. Martinez ME, Willett WC. Calcium, vitamin D, and colorectal cancer. A review of the epidemiological evidence. Cancer Epidemiol Biomarkers Prev 1998; 7:163-8.
64. Liu G, Hu X, Chakrabarty S. Vitamin D mediates its action in human colon carcinoma cells in a calcium-sensing receptor-dependent manner: downregulates malignant cell behavior and the expression of thymidylate synthase and survivin and promotes cellular sensitivity to 5-FU. Int J Cancer 2010; 126:631-9.