|
|
||||||||
1 Departments of Cell Biology and of Physiology and Biophysics and Gregory Fleming James Cystic Fibrosis Research Center, University of Alabama, Birmingham, Alabama 35294-0005; 2 Department of Laboratory Medicine, Cardiovascular Research Institute, University of California, San Francisco, California 94143-0911; and 3 Departments of Physiology and Pediatrics and Cystic Fibrosis Research Center, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
Autocrine and paracrine release of and extracellular signaling by ATP is a ubiquitous cell biological and physiological process. Despite this knowledge, the mechanisms and physiological roles of cellular ATP release are unknown. We tested the hypothesis that epithelia release ATP under basal and stimulated conditions by using a newly designed and highly sensitive assay for bioluminescence detection of ATP released from polarized epithelial monolayers. This bioluminescence assay measures ATP released from cystic fibrosis (CF) and non-CF human epithelial monolayers in a reduced serum medium through catalysis of the luciferase-luciferin reaction, yielding a photon of light collected by a luminometer. This novel assay measures ATP released into the apical or basolateral medium surrounding epithelia. Of relevance to CF, CF epithelia fail to release ATP across the apical membrane under basal conditions. Moreover, hypotonicity is an extracellular signal that stimulates ATP release into both compartments of non-CF epithelia in a reversible manner; the response to hypotonicity is also lost in CF epithelia. The bioluminescence detection assay for ATP released from epithelia and other cells will be useful in the study of extracellular nucleotide signaling in physiological and pathophysiological paradigms. Taken together, these results suggest that extracellular ATP may be a constant regulator of epithelial cell function under basal conditions and an autocrine regulator of cell volume under hypotonic conditions, two functions that may be lost in CF and contribute to CF pathophysiology.
extracellular nucleotides; autocrine and paracrine regulation; airway; signaling; ecto-adenosinetriphosphatase; cell culture; cell volume regulation
This article has been cited by other articles:
![]() |
K. Woo, A. K. Dutta, V. Patel, C. Kresge, and A. P. Feranchak Fluid flow induces mechanosensitive ATP release, calcium signalling and Cl- transport in biliary epithelial cells through a PKC{zeta}-dependent pathway J. Physiol., June 1, 2008; 586(11): 2779 - 2798. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Vallon P2 receptors in the regulation of renal transport mechanisms Am J Physiol Renal Physiol, January 1, 2008; 294(1): F10 - F27. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Olteanu, M. B. Hovater, and E. M. Schwiebert Intraluminal autocrine purinergic signaling within cysts: implications for the progression of diseases that involve encapsulated cyst formation Am J Physiol Renal Physiol, January 1, 2007; 292(1): F11 - F14. [Full Text] [PDF] |
||||
![]() |
S. A. Lewis and J. R. Lewis Kinetics of urothelial ATP release Am J Physiol Renal Physiol, August 1, 2006; 291(2): F332 - F340. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Sun and T. C. Chai Augmented extracellular ATP signaling in bladder urothelial cells from patients with interstitial cystitis Am J Physiol Cell Physiol, January 1, 2006; 290(1): C27 - C34. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Blumenthal Modulation of tyramine signaling by osmolality in an insect secretory epithelium Am J Physiol Cell Physiol, November 1, 2005; 289(5): C1261 - C1267. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. K. Crane, T. M. Naeher, S. S. Choudhari, and E. M. Giroux Two pathways for ATP release from host cells in enteropathogenic Escherichia coli infection Am J Physiol Gastrointest Liver Physiol, September 1, 2005; 289(3): G407 - G417. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Komlosi, A. Fintha, and P. D. Bell Renal Cell-to-Cell Communication via Extracellular ATP Physiology, April 1, 2005; 20(2): 86 - 90. [Abstract] [Full Text] [PDF] |
||||
![]() |
Q. Wang, L. Wang, Y.-H. Feng, X. Li, R. Zeng, and G. I. Gorodeski P2X7 receptor-mediated apoptosis of human cervical epithelial cells Am J Physiol Cell Physiol, November 1, 2004; 287(5): C1349 - C1358. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Gatof, G. Kilic, and J. G. Fitz Vesicular exocytosis contributes to volume-sensitive ATP release in biliary cells Am J Physiol Gastrointest Liver Physiol, April 1, 2004; 286(4): G538 - G546. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Schafer, F. Sedehizade, T. Welte, and G. Reiser ATP- and UTP-activated P2Y receptors differently regulate proliferation of human lung epithelial tumor cells Am J Physiol Lung Cell Mol Physiol, August 1, 2003; 285(2): L376 - L385. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. M. Joseph, M. R. Buchakjian, and G. R. Dubyak Colocalization of ATP Release Sites and Ecto-ATPase Activity at the Extracellular Surface of Human Astrocytes J. Biol. Chem., June 20, 2003; 278(26): 23331 - 23342. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. J. Cooke, J. Wunderlich, and F. L. Christofi "The Force Be with You": ATP in Gut Mechanosensory Transduction Physiology, April 1, 2003; 18(2): 43 - 49. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Leipziger Control of epithelial transport via luminal P2 receptors Am J Physiol Renal Physiol, March 1, 2003; 284(3): F419 - F432. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. B. Woda, M. Leite Jr., R. Rohatgi, and L. M. Satlin Effects of luminal flow and nucleotides on [Ca2+]i in rabbit cortical collecting duct Am J Physiol Renal Physiol, September 1, 2002; 283(3): F437 - F446. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Yamamoto and Y. Suzuki Role of luminal ATP in regulating electrogenic Na+ absorption in guinea pig distal colon Am J Physiol Gastrointest Liver Physiol, August 1, 2002; 283(2): G300 - G308. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. H.-Y. Wong and W.-h. Ko Stimulation of Cl- Secretion via Membrane-restricted Ca2+ Signaling Mediated by P2Y Receptors in Polarized Epithelia J. Biol. Chem., March 8, 2002; 277(11): 9016 - 9021. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. C. Fleischhauer, C. H. Mitchell, K. Peterson-Yantorno, M. Coca-Prados, and M. M. Civan PGE2, Ca2+, and cAMP mediate ATP activation of Cl- channels in pigmented ciliary epithelial cells Am J Physiol Cell Physiol, November 1, 2001; 281(5): C1614 - C1623. [Abstract] [Full Text] [PDF] |
||||
![]() |
L.-J. Dai, H. S. Kang, D. Kerstan, G. Ritchie, and G. A. Quamme ATP inhibits Mg2+ uptake in MDCT cells via P2X purinoceptors Am J Physiol Renal Physiol, November 1, 2001; 281(5): F833 - F840. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. W. Inscho P2 receptors in regulation of renal microvascular function Am J Physiol Renal Physiol, June 1, 2001; 280(6): F927 - F944. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Schwiebert and B. K. Kishore Extracellular nucleotide signaling along the renal epithelium Am J Physiol Renal Physiol, June 1, 2001; 280(6): F945 - F963. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. P. Hamill and B. Martinac Molecular Basis of Mechanotransduction in Living Cells Physiol Rev, April 1, 2001; 81(2): 685 - 740. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Vassort Adenosine 5'-Triphosphate: a P2-Purinergic Agonist in the Myocardium Physiol Rev, April 1, 2001; 81(2): 767 - 806. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Nishiyama, D. S. A. Majid, M. Walker III, A. Miyatake, and L. G. Navar Renal Interstitial ATP Responses to Changes in Arterial Pressure During Alterations in Tubuloglomerular Feedback Activity Hypertension, February 1, 2001; 37(2): 753 - 759. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Schwiebert Extracellular ATP-mediated propagation of Ca2+ waves.Focus on "Mechanical strain-induced Am J Physiol Cell Physiol, August 1, 2000; 279(2): C281 - C283. [Full Text] [PDF] |
||||
![]() |
A. Nishiyama, D. S. A. Majid, K. A. Taher, A. Miyatake, and L. G. Navar Relation Between Renal Interstitial ATP Concentrations and Autoregulation-Mediated Changes in Renal Vascular Resistance Circ. Res., March 31, 2000; 86(6): 656 - 662. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. D. Salter, J. G. Fitz, and R. M. Roman Domain-specific purinergic signaling in polarized rat cholangiocytes Am J Physiol Gastrointest Liver Physiol, March 1, 2000; 278(3): G492 - G500. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. M. Roman, A. P. Feranchak, A. K. Davison, E. M. Schwiebert, and J. G. Fitz Evidence for Gd3+ inhibition of membrane ATP permeability and purinergic signaling Am J Physiol Gastrointest Liver Physiol, December 1, 1999; 277(6): G1222 - G1230. [Abstract] [Full Text] [PDF] |
||||
![]() |
K.-I. Hosoya, H. Ueda, K.-J. Kim, and V. H. L. Lee Nucleotide Stimulation of Cl- Secretion in the Pigmented Rabbit Conjunctiva J. Pharmacol. Exp. Ther., October 1, 1999; 291(1): 53 - 59. [Abstract] [Full Text] |
||||
![]() |
D. B. Light, T. L. Capes, R. T. Gronau, and M. R. Adler Extracellular ATP stimulates volume decrease in Necturus red blood cells Am J Physiol Cell Physiol, September 1, 1999; 277(3): C480 - C491. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. M. Roman, A. P. Feranchak, K. D. Salter, Y. Wang, and J. G. Fitz Endogenous ATP release regulates Cl- secretion in cultured human and rat biliary epithelial cells Am J Physiol Gastrointest Liver Physiol, June 1, 1999; 276(6): G1391 - G1400. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Schwiebert ABC transporter-facilitated ATP conductive transport Am J Physiol Cell Physiol, January 1, 1999; 276(1): C1 - C8. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Boudreault and R. Grygorczyk Cell swelling-induced ATP release and gadolinium-sensitive channels Am J Physiol Cell Physiol, January 1, 2002; 282(1): C219 - C226. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. M. Schwiebert, W. C. Rice, B. A. Kudlow, A. L. Taylor, and E. M. Schwiebert Extracellular ATP signaling and P2X nucleotide receptors in monolayers of primary human vascular endothelial cells Am J Physiol Cell Physiol, February 1, 2002; 282(2): C289 - C301. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. Schwiebert, D. P. Wallace, G. M. Braunstein, S. R. King, J. Peti-Peterdi, K. Hanaoka, W. B. Guggino, L. M. Guay-Woodford, P. D. Bell, L. P. Sullivan, et al. Autocrine extracellular purinergic signaling in epithelial cells derived from polycystic kidneys Am J Physiol Renal Physiol, April 1, 2002; 282(4): F763 - F775. [Abstract] [Full Text] [PDF] |
||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |