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J Biol Chem, Vol. 274, Issue 32, 22739-22746, August 6, 1999

Molecular Cloning and Characterization of a Channel-like Transporter Mediating Intestinal Calcium Absorption

Ji-Bin Peng^§, Xing-Zhen Chen^§, Urs V. Berger^§, Peter M. Vassilev^**, Hiroyasu Tsukaguchi^§, Edward M. Brown^**, and Matthias A. Hediger^§

From the  Membrane Biology Program and the ^§ Renal and ^** Endocrine-Hypertension Divisions, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts 02115

Calcium is a major component of the mineral phase of bone and serves as a key intracellular second messenger. Postnatally, all bodily calcium must be absorbed from the diet through the intestine. Here we report the properties of a calcium transport protein (CaT1) cloned from rat duodenum using an expression cloning strategy in Xenopus laevis oocytes, which likely plays a key role in the intestinal uptake of calcium. CaT1 shows homology (75% amino acid sequence identity) to the apical calcium channel ECaC recently cloned from vitamin D-responsive cells of rabbit kidney and is structurally related to the capsaicin receptor and the TRP family of ion channels. Based on Northern analysis of rat tissues, a 3-kilobase CaT1 transcript is present in rat duodenum, proximal jejunum, cecum, and colon, and a 6.5-kilobase transcript is present in brain, thymus, and adrenal gland. In situ hybridization revealed strong CaT1 mRNA expression in enterocytes of duodenum, proximal jejunum, and cecum. No signals were detected in kidney, heart, liver, lung, spleen, and skeletal muscle. When expressed in Xenopus oocytes, CaT1 mediates saturable Ca²⁺ uptake with a Michaelis constant of 0.44 mM. Transport of Ca²⁺ by CaT1 is electrogenic, voltage-dependent, and exhibits a charge/Ca²⁺ uptake ratio close to 2:1, indicating that CaT1-mediated Ca²⁺ influx is not coupled to other ions. CaT1 activity is pH-sensitive, exhibiting significant inhibition by low pH. CaT1 is also permeant to Sr²⁺ and Ba²⁺ (but not Mg²⁺), although the currents evoked by Sr²⁺ and Ba²⁺ are much smaller than those evoked by Ca²⁺. The trivalent cations Gd³⁺ and La³⁺ and the divalent cations Cu²⁺, Pb²⁺, Cd²⁺, Co²⁺, and Ni²⁺ (each at 100 µM) do not evoke currents themselves, but inhibit CaT1-mediated Ca²⁺ transport. Fe³⁺, Fe²⁺, Mn²⁺, and Zn²⁺ have no significant effects at 100 µM on CaT1-mediated Ca²⁺ transport. CaT1 mRNA levels are not responsive to 1,25-dihydroxyvitamin D₃ administration or to calcium deficiency. Our studies strongly suggest that CaT1 provides the principal mechanism for Ca²⁺ entry into enterocytes as part of the transcellular pathway of calcium absorption in the intestine.

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				J. G J Hoenderop, R. Vennekens, D. Muller, J. Prenen, G. Droogmans, R. J M Bindels, and B. Nilius Function and expression of the epithelial Ca2+ channel family: comparison of mammalian ECaC1 and 2 J. Physiol., December 15, 2001; 537(3): 747 - 761. [Abstract] [Full Text] [PDF]

				T. Voets, J. Prenen, A. Fleig, R. Vennekens, H. Watanabe, J. G. J. Hoenderop, R. J. M. Bindels, G. Droogmans, R. Penner, and B. Nilius CaT1 and the Calcium Release-activated Calcium Channel Manifest Distinct Pore Properties J. Biol. Chem., December 14, 2001; 276(51): 47767 - 47770. [Abstract] [Full Text] [PDF]

				S. J. Van Cromphaut, M. Dewerchin, J. G. J. Hoenderop, I. Stockmans, E. Van Herck, S. Kato, R. J. M. Bindels, D. Collen, P. Carmeliet, R. Bouillon, et al. Duodenal calcium absorption in vitamin D receptor-knockout mice: Functional and molecular aspects PNAS, October 25, 2001; (2001) 231474698. [Abstract] [Full Text] [PDF]

				B. S. Fischer, D. Qin, K. Kim, and T. V. McDonald Capsaicin Inhibits Jurkat T-Cell Activation by Blocking Calcium Entry Current ICRAC J. Pharmacol. Exp. Ther., October 1, 2001; 299(1): 238 - 246. [Abstract] [Full Text] [PDF]

				D. Muller, J. G. J. Hoenderop, C. H. van Os, and R. J. M. Bindels The epithelial calcium channel, ECaC1: molecular details of a novel player in renal calcium handling Nephrol. Dial. Transplant., July 1, 2001; 16(7): 1329 - 1335. [Full Text] [PDF]

				B. M. Slepchenko and F. Bronner Modeling of transcellular Ca transport in rat duodenum points to coexistence of two mechanisms of apical entry Am J Physiol Cell Physiol, July 1, 2001; 281(1): C270 - C281. [Abstract] [Full Text] [PDF]

				P. Lane, G. Hao, and S. S. Gross S-Nitrosylation Is Emerging as a Specific and Fundamental Posttranslational Protein Modification: Head-to-Head Comparison with O-Phosphorylation Sci. Signal., June 12, 2001; 2001(86): re1 - re1. [Abstract] [Full Text] [PDF]

				L. Valencia, M. Bidet, S. Martial, E. Sanchez, E. Melendez, M. Tauc, C. Poujeol, D. Martin, M. D. C. Namorado, J. L. Reyes, et al. Nifedipine-activated Ca2+ permeability in newborn rat cortical collecting duct cells in primary culture Am J Physiol Cell Physiol, May 1, 2001; 280(5): C1193 - C1203. [Abstract] [Full Text] [PDF]

				B. A. Niemeyer, C. Bergs, U. Wissenbach, V. Flockerzi, and C. Trost Competitive regulation of CaT-like-mediated Ca2+ entry by protein kinase C and calmodulin PNAS, March 13, 2001; 98(6): 3600 - 3605. [Abstract] [Full Text] [PDF]

				N. F. Barley, A. Howard, D. O'Callaghan, S. Legon, and J. R. F. Walters Epithelial calcium transporter expression in human duodenum Am J Physiol Gastrointest Liver Physiol, February 1, 2001; 280(2): G285 - G290. [Abstract] [Full Text] [PDF]

				N. S. DELANY, M. HURLE, P. FACER, T. ALNADAF, C. PLUMPTON, I. KINGHORN, C. G. SEE, M. COSTIGAN, P. ANAND, C. J. WOOLF, et al. Identification and characterization of a novel human vanilloid receptor-like protein, VRL-2 Physiol Genomics, January 19, 2001; 4(3): 165 - 174. [Abstract] [Full Text] [PDF]

				E. M. Brown and R. J. MacLeod Extracellular Calcium Sensing and Extracellular Calcium Signaling Physiol Rev, January 1, 2001; 81(1): 239 - 297. [Abstract] [Full Text] [PDF]

				B. Nilius, R. Vennekens, J. Prenen, J. G J Hoenderop, R. J M Bindels, and G. Droogmans Whole-cell and single channel monovalent cation currents through the novel rabbit epithelial Ca2+ channel ECaC J. Physiol., September 1, 2000; 527(2): 239 - 248. [Abstract] [Full Text] [PDF]

				R. Vennekens, J. G. J. Hoenderop, J. Prenen, M. Stuiver, P. H. G. M. Willems, G. Droogmans, B. Nilius, and R. J. M. Bindels Permeation and Gating Properties of the Novel Epithelial Ca2+ Channel J. Biol. Chem., February 11, 2000; 275(6): 3963 - 3969. [Abstract] [Full Text] [PDF]

				M. J. Hubbard Calcium Transport Across the Dental Enamel Epithelium Critical Reviews in Oral Biology & Medicine, January 1, 2000; 11(4): 437 - 466. [Abstract] [Full Text] [PDF]

				U. Wissenbach, B. A. Niemeyer, T. Fixemer, A. Schneidewind, C. Trost, A. Cavalie, K. Reus, E. Meese, H. Bonkhoff, and V. Flockerzi Expression of CaT-like, a Novel Calcium-selective Channel, Correlates with the Malignancy of Prostate Cancer J. Biol. Chem., May 25, 2001; 276(22): 19461 - 19468. [Abstract] [Full Text] [PDF]

				X. Liu and I. S. Ambudkar Characteristics of a Store-operated Calcium-permeable Channel. SARCOENDOPLASMIC RETICULUM CALCIUM PUMP FUNCTION CONTROLS CHANNEL GATING J. Biol. Chem., August 3, 2001; 276(32): 29891 - 29898. [Abstract] [Full Text] [PDF]

				J.-B. Peng, X.-Z. Chen, U. V. Berger, P. M. Vassilev, E. M. Brown, and M. A. Hediger A Rat Kidney-specific Calcium Transporter in the Distal Nephron J. Biol. Chem., September 1, 2000; 275(36): 28186 - 28194. [Abstract] [Full Text] [PDF]

				S. J. Van Cromphaut, M. Dewerchin, J. G. J. Hoenderop, I. Stockmans, E. Van Herck, S. Kato, R. J. M. Bindels, D. Collen, P. Carmeliet, R. Bouillon, et al. Duodenal calcium absorption in vitamin D receptor-knockout mice: Functional and molecular aspects PNAS, November 6, 2001; 98(23): 13324 - 13329. [Abstract] [Full Text] [PDF]

				A. Manninen and K. Saksela HIV-1 Nef Interacts with Inositol Trisphosphate Receptor to Activate Calcium Signaling in T Cells J. Exp. Med., April 15, 2002; 195(8): 1023 - 1032. [Abstract] [Full Text] [PDF]

				K. Jean, G. Bernatchez, H. Klein, L. Garneau, R. Sauve, and L. Parent Role of aspartate residues in Ca2+ affinity and permeation of the distal ECaC1 Am J Physiol Cell Physiol, April 1, 2002; 282(4): C665 - C672. [Abstract] [Full Text] [PDF]