|
Journal of Histochemistry and Cytochemistry, Vol. 46, 205-214, Copyright © 1998 by The Histochemical Society, Inc.
Basolateral Distribution of Caveolin-1 in the Kidney: Absence from H+-ATPase-coated Endocytic Vesicles in Intercalated Cells
Sylvie Bretona,
Michael P. Lisanti1,b,
Robert Tyszkowskia,
Margaret McLaughlina, and
Dennis Browna
a Renal Unit and Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
b Whitehead Institute for Biomedical Research, Cambridge, Massachusetts
Correspondence to:
Sylvie Breton, Renal Unit, Massachusetts General Hospital East, 149 13th St., Charlestown, MA 02129.
In kidney epithelial cells, a variety of physiological processes are dependent on the active recycling of membrane proteins between intracellular vesicles and the cell surface. Although clathrin-mediated endocytosis occurs in several renal cell types, endocytosis can also occur by non-clathrin-coated vesicles, including pinocytotic structures known as caveolae that contain a novel coat protein, caveolin. Exo- and endocytosis of a vacuolar H+-ATPase in intercalated cells also occurs via specialized "coated" vesicles that do not contain clathrin. The aim of this study was to localize caveolin in the kidney and, in addition, to determine whether it could be a component of the H+-ATPase recycling process. Using an antibody against the - and ß-isoforms of caveolin-1, our immunocytochemical data show a marked heterogeneity in the cellular expression of this isoform of caveolin in kidney. In contrast, caveolin-3 was not detectable in renal epithelial cells. Caveolin-1 was abundant in endothelial cells and smooth muscle cells and was present in the parietal cells of Bowman's capsule. Distal tubule cells, connecting tubule cells, and collecting duct principal cells exhibited marked punctate basolateral staining, corresponding to the presence of caveolae detected by electron microscopy, whereas all intercalated cells were negative in both cortex and medulla. These data indicate that although caveolin-1 may participate in basolateral events in some kidney epithelial cell types, it does not appear to be involved in the regulated recycling of H+-ATPase in intercalated cells. Therefore, these cells recycle H+-ATPase by a mechanism that involves neither clathrin nor caveolin-1. (J Histochem Cytochem 46:205214, 1998)
Key Words:
immunocytochemistry, caveolin, kidney, intercalated cell, endocytosis

CiteULike Complore Connotea Del.icio.us Digg Reddit Technorati What's this?
This article has been cited by other articles:

|
 |

|
 |
 
Z. Cao, C. Li, J. N. Higginbotham, J. L. Franklin, D. L. Tabb, R. Graves-Deal, S. Hill, K. Cheek, W. G. Jerome, L. A. Lapierre, et al.
Use of Fluorescence-activated Vesicle Sorting for Isolation of Naked2-associated, Basolaterally Targeted Exocytic Vesicles for Proteomics Analysis
Mol. Cell. Proteomics,
September 1, 2008;
7(9):
1651 - 1667.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Welker, A. Bohlick, K. Mutig, M. Salanova, T. Kahl, H. Schluter, D. Blottner, J. Ponce-Coria, G. Gamba, and S. Bachmann
Renal Na+-K+-Cl- cotransporter activity and vasopressin-induced trafficking are lipid raft-dependent
Am J Physiol Renal Physiol,
September 1, 2008;
295(3):
F789 - F802.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Han, H. Li, V. A. M. Villar, A. M. Pascua, M. I. Dajani, X. Wang, A. Natarajan, M. T. Quinn, R. A. Felder, P. A. Jose, et al.
Lipid Rafts Keep NADPH Oxidase in the Inactive State in Human Renal Proximal Tubule Cells
Hypertension,
February 1, 2008;
51(2):
481 - 487.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Willoughby and D. M. F. Cooper
Organization and Ca2+ Regulation of Adenylyl Cyclases in cAMP Microdomains
Physiol Rev,
July 1, 2007;
87(3):
965 - 1010.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Welker, B. Geist, J.-H. Fruhauf, M. Salanova, D. A. Groneberg, E. Krause, and S. Bachmann
Role of lipid rafts in membrane delivery of renal epithelial Na+-K+-ATPase, thick ascending limb
Am J Physiol Regulatory Integrative Comp Physiol,
March 1, 2007;
292(3):
R1328 - R1337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Breton and D. Brown
New insights into the regulation of V-ATPase-dependent proton secretion
Am J Physiol Renal Physiol,
January 1, 2007;
292(1):
F1 - F10.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Ullrich, A. Caplanusi, B. Brone, D. Hermans, E. Lariviere, B. Nilius, W. Van Driessche, and J. Eggermont
Stimulation by caveolin-1 of the hypotonicity-induced release of taurine and ATP at basolateral, but not apical, membrane of Caco-2 cells
Am J Physiol Cell Physiol,
May 1, 2006;
290(5):
C1287 - C1296.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. C. Mora, V. L. Bonilha, B.-C. Shin, J. Hu, L. Cohen-Gould, D. Bok, and E. Rodriguez-Boulan
Bipolar assembly of caveolae in retinal pigment epithelium
Am J Physiol Cell Physiol,
March 1, 2006;
290(3):
C832 - C843.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Pastor-Soler, C. Pietrement, and S. Breton
Role of Acid/Base Transporters in the Male Reproductive Tract and Potential Consequences of Their Malfunction
Physiology,
December 1, 2005;
20(6):
417 - 428.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Willoughby, N. Masada, A. J. Crossthwaite, A. Ciruela, and D. M. F. Cooper
Localized Na+/H+ Exchanger 1 Expression Protects Ca2+-regulated Adenylyl Cyclases from Changes in Intracellular pH
J. Biol. Chem.,
September 2, 2005;
280(35):
30864 - 30872.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Beaulieu, N. Da Silva, N. Pastor-Soler, C. R. Brown, P. J. S. Smith, D. Brown, and S. Breton
Modulation of the Actin Cytoskeleton via Gelsolin Regulates Vacuolar H+-ATPase Recycling
J. Biol. Chem.,
March 4, 2005;
280(9):
8452 - 8463.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Trivedi, V. A. Narkar, T. Hussain, and M. F. Lokhandwala
Dopamine recruits D1A receptors to Na-K-ATPase-rich caveolar plasma membranes in rat renal proximal tubules
Am J Physiol Renal Physiol,
November 1, 2004;
287(5):
F921 - F931.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Ferrandi, I. Molinari, P. Barassi, E. Minotti, G. Bianchi, and P. Ferrari
Organ Hypertrophic Signaling within Caveolae Membrane Subdomains Triggered by Ouabain and Antagonized by PST 2238
J. Biol. Chem.,
August 6, 2004;
279(32):
33306 - 33314.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. M. Sandoval, M. D. Kennedy, P. S. Low, and B. A. Molitoris
Uptake and trafficking of fluorescent conjugates of folic acid in intact kidney determined using intravital two-photon microscopy
Am J Physiol Cell Physiol,
August 1, 2004;
287(2):
C517 - C526.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. El Annan, D. Brown, S. Breton, S. Bourgoin, D. A. Ausiello, and V. Marshansky
Differential expression and targeting of endogenous Arf1 and Arf6 small GTPases in kidney epithelial cells in situ
Am J Physiol Cell Physiol,
April 1, 2004;
286(4):
C768 - C778.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. L. TUMA and A. L. HUBBARD
Transcytosis: Crossing Cellular Barriers
Physiol Rev,
July 1, 2003;
83(3):
871 - 932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Capozza, T. M. Williams, W. Schubert, S. McClain, B. Bouzahzah, F. Sotgia, and M. P. Lisanti
Absence of Caveolin-1 Sensitizes Mouse Skin to Carcinogen-Induced Epidermal Hyperplasia and Tumor Formation
Am. J. Pathol.,
June 1, 2003;
162(6):
2029 - 2039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Loffing and B. Kaissling
Sodium and calcium transport pathways along the mammalian distal nephron: from rabbit to human
Am J Physiol Renal Physiol,
April 1, 2003;
284(4):
F628 - F643.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Cao, G. Yang, T. L. Timme, T. Saika, L. D. Truong, T. Satoh, A. Goltsov, S. H. Park, T. Men, N. Kusaka, et al.
Disruption of the Caveolin-1 Gene Impairs Renal Calcium Reabsorption and Leads to Hypercalciuria and Urolithiasis
Am. J. Pathol.,
April 1, 2003;
162(4):
1241 - 1248.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Sorensson, W. Fierlbeck, T. Heider, K. Schwarz, D. S. Park, P. Mundel, M. Lisanti, and B. J. Ballermann
Glomerular Endothelial Fenestrae In Vivo Are Not Formed from Caveolae
J. Am. Soc. Nephrol.,
November 1, 2002;
13(11):
2639 - 2647.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Badizadegan, B. L. Dickinson, H. E. Wheeler, R. S. Blumberg, R. K. Holmes, and W. I. Lencer
Heterogeneity of detergent-insoluble membranes from human intestine containing caveolin-1 and ganglioside GM1
Am J Physiol Gastrointest Liver Physiol,
June 1, 2000;
278(6):
G895 - G904.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Breton, N. N. Nsumu, T. Galli, I. Sabolic, P. J. S. Smith, and D. Brown
Tetanus toxin-mediated cleavage of cellubrevin inhibits proton secretion in the male reproductive tract
Am J Physiol Renal Physiol,
May 1, 2000;
278(5):
F717 - F725.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Murthy, L. A. Haddad, N. Smith, D. Pinney, R. Tyszkowski, D. Brown, and V. Ramesh
Similarities and differences in the subcellular localization of hamartin and tuberin in the kidney
Am J Physiol Renal Physiol,
May 1, 2000;
278(5):
F737 - F746.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. L. Stevens, S. Breton, C. E. Gustafson, R. Bouley, R. D. Nelson, D. E. Kohan, and D. Brown
Aquaporin 2 is a vasopressin-independent, constitutive apical membrane protein in rat vas deferens
Am J Physiol Cell Physiol,
April 1, 2000;
278(4):
C791 - C802.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Brown
Targeting of membrane transporters in renal epithelia: when cell biology meets physiology
Am J Physiol Renal Physiol,
February 1, 2000;
278(2):
F192 - F201.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D Brown and S Breton
H(+)V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways
J. Exp. Biol.,
January 1, 2000;
203(1):
137 - 145.
[Abstract]
|
 |
|

|
 |

|
 |
 
R. Mora, V. L. Bonilha, A. Marmorstein, P. E. Scherer, D. Brown, M. P. Lisanti, and E. Rodriguez-Boulan
Caveolin-2 Localizes to the Golgi Complex but Redistributes to Plasma Membrane, Caveolae, and Rafts when Co-expressed with Caveolin-1
J. Biol. Chem.,
September 3, 1999;
274(36):
25708 - 25717.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Bradbury, J. A. Clark, S. C. Watkins, C. C. Widnell, H. S. Smith IV, and R. J. Bridges
Characterization of the internalization pathways for the cystic fibrosis transmembrane conductance regulator
Am J Physiol Lung Cell Mol Physiol,
April 1, 1999;
276(4):
L659 - L668.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Breton, T. Inoue, M. A. Knepper, and D. Brown
Antigen retrieval reveals widespread basolateral expression of syntaxin 3 in renal epithelia
Am J Physiol Renal Physiol,
March 1, 2002;
282(3):
F523 - F529.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.-X. Sun, A. Van Hoek, Y. Huang, R. Bouley, M. McLaughlin, and D. Brown
Aquaporin-2 localization in clathrin-coated pits: inhibition of endocytosis by dominant-negative dynamin
Am J Physiol Renal Physiol,
June 1, 2002;
282(6):
F998 - F1011.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Biemesderfer, S. A. Mentone, M. Mooseker, and T. Hasson
Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules
Am J Physiol Renal Physiol,
May 1, 2002;
282(5):
F785 - F794.
[Abstract]
[Full Text]
[PDF]
|
 |
|
The Journal of Histochemistry & Cytochemistry
is owned, published, and licensed by
The Histochemical Society © 1998
|
|
|