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PMID: 15477379 Published · ppublish English Journal Article

Voltage-dependent anion channel-1 (VDAC-1) contributes to ATP release and cell volume regulation in murine cells.

The Journal of general physiology ·Vol. 124 ·No. 5 ·2004-11-00 ·Pages 513-26

Okada SF, O'Neal WK, Huang P, Nicholas RA, Ostrowski LE, Craigen WJ, Lazarowski ER, Boucher RC

Abstract

Extracellular ATP regulates several elements of the mucus clearance process important for pulmonary host defense. However, the mechanisms mediating ATP release onto airway surfaces remain unknown. Mitochondrial voltage-dependent anion channels (mt-VDACs) translocate a variety of metabolites, including ATP and ADP, across the mitochondrial outer membrane, and a plasmalemmal splice variant (pl-VDAC-1) has been proposed to mediate ATP translocation across the plasma membrane. We tested the involvement of VDAC-1 in ATP release in a series of studies in murine cells. First, the full-length coding sequence was cloned from a mouse airway epithelial cell line (MTE7b-) and transfected into NIH 3T3 cells, and pl-VDAC-1-transfected cells exhibited higher rates of ATP release in response to medium change compared with mock-transfected cells. Second, ATP release was compared in cells isolated from VDAC-1 knockout [VDAC-1 (-/-)] and wild-type (WT) mice. Fibroblasts from VDAC-1 (-/-) mice released less ATP than WT mice in response to a medium change. Well-differentiated cultures from nasal and tracheal epithelia of VDAC-1 (-/-) mice exhibited less ATP release in response to luminal hypotonic challenge than WT mice. Confocal microscopy studies revealed that cell volume acutely increased in airway epithelia from both VDAC-1 (-/-) and WT mice after luminal hypotonic challenge, but VDAC-1 (-/-) cells exhibited a slower regulatory volume decrease (RVD) than WT cells. Addition of ATP or apyrase to the luminal surface of VDAC-1 (-/-) or WT cultures with hypotonic challenge produced similar initial cell height responses and RVD kinetics in both cell types, suggesting that involvement of VDAC-1 in RVD is through ATP release. Taken together, these studies suggest that VDAC-1, directly or indirectly, contributes to ATP release from murine cells. However, the observation that VDAC-1 knockout cells released a significant amount of ATP suggests that other molecules also play a role in this function.

MeSH Terms
Adenosine Triphosphate/pharmacokinetics Animals Cell Size Cells, Cultured Cloning, Molecular Ion Channel Gating/physiology Mice NIH 3T3 Cells Osmotic Pressure Porins/physiology Recombinant Proteins/metabolism Respiratory Mucosa/cytology,physiology Voltage-Dependent Anion Channel 1 Voltage-Dependent Anion Channels Water-Electrolyte Balance/physiology
Chemicals
Porins Recombinant Proteins Vdac1 protein, mouse Voltage-Dependent Anion Channels Adenosine Triphosphate Voltage-Dependent Anion Channel 1
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Okada Seiko F
Cystic Fibrosis/Pulmonary Research and Treatment Center, The University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. [email protected]
O'Neal Wanda K
Huang Pingbo
Nicholas Robert A
Ostrowski Lawrence E
Craigen William J
Lazarowski Eduardo R
Boucher Richard C
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Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
DOI
10.1085/jgp.200409154
Email
[email protected]
Published
2004-11-00
Epub
2004-00-11
Pages
513-26
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2234005
Subset
IM
Grants
NHLBI NIH HHS · P01 HL034322 · United States
External Links
PubMed source DOI: 10.1085/jgp.200409154 PMC Full Text View journal details
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