Immunolocalization of Caveolin-1 in Rat and Human Mesothelium

Flask-shaped vesicles have been described as caveolae in mesothelial cells in a number of animal species based on morphological criteria only. Using an antibody against caveolin-1, said to be a biochemical marker of caveolae, immunoelectron microscopy suggests that many but not all such vesicles in mesothelial cells are caveolae. Mesothelial cells from different anatomical sites showed obvious variations in both the population density and distribution of these flask-shaped vesicles and in their density of immunostaining. Lung and pericardial sac had the highest staining density. In some sites (e.g., lung, bladder, colon) caveolae were equally distributed between apical and basolateral surfaces, whereas in others (e.g., spleen, liver), they were predominantly apical. Additional immunopositive sites in the peritoneal membrane were identified, including the epineurium of peripheral nerves and the endothelium of lymphatic vessels. We further suggest that variations in the number of mesothelial cell caveolae and the density of their immunolabeling may have implications for our understanding of certain diseases such as malignant mesothelioma, especially in view of the recent hypothesis that it may be caused by SV40, a virus that appears to enter cells via caveolae.

[1]  B. Jasani,et al.  Silver Development in Microscopy and Bioanalysis: a New Versatile Formulation for Modern Needs , 1998, The Histochemical Journal.

[2]  J. Kay,et al.  Immunogold electron-microscopic localisation of calpain I in skeletal muscle of rats , 2004, Cell and Tissue Research.

[3]  John D. Williams,et al.  Can Artifact Mimic the Pathology of the Peritoneal Mesothelium? , 2003, Peritoneal dialysis international : journal of the International Society for Peritoneal Dialysis.

[4]  R. Garcea,et al.  Simian Virus 40 Infection of Humans , 2003, Journal of Virology.

[5]  Yasuhiro Ito,et al.  Malignant mesothelioma of the pericardium: Case reports and immunohistochemical studies including Ki‐67 expression , 2002, Pathology international.

[6]  H. Ballard,et al.  Evidence For The Existence Of A Constitutive Nitric Oxide Synthase In Vascular Smooth Muscle , 2002, Clinical and experimental pharmacology & physiology.

[7]  Stephen W Carmichael,et al.  Localization of Caveolin 1 in Aortic Valve Endothelial Cells Using Antigen Retrieval , 2002, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[8]  D. Gruenert,et al.  SV40, growth factors, and mesothelioma: another piece of the puzzle. , 2002, American journal of respiratory cell and molecular biology.

[9]  M. Lisanti,et al.  Withdrawal of “Caveolae and Their Coat Proteins, the Caveolins: From Electron Microscopic Novelty to Biological Launching Pad” [Journal of Cellular Physiology 186(3) 329‐337 (2001)] , 2001, Journal of cellular physiology.

[10]  D. Gruenert,et al.  Another Piece of the Puzzle , 2002 .

[11]  J. Testa,et al.  Detection of SV40 DNA sequences in malignant mesothelioma specimens from the United States, but not from Turkey , 2002, Journal of cellular biochemistry.

[12]  J. Couet,et al.  Cell biology of caveolae and caveolin. , 2001, Advanced drug delivery reviews.

[13]  Lucas Pelkmans,et al.  Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER , 2001, Nature Cell Biology.

[14]  O. Devuyst,et al.  Regulation of NO synthase isoforms in the peritoneum: implications for ultrafiltration failure in peritoneal dialysis. , 2001, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[15]  A. Gazdar,et al.  Association of SV40 with human tumours. , 2001, Seminars in cancer biology.

[16]  K. Rundell,et al.  The role of the SV40 ST antigen in cell growth promotion and transformation. , 2001, Seminars in cancer biology.

[17]  K. Michailova Electronmicroscopic observations on the visceral and parietal rat's pleura after contralateral pneumonectomy. , 2001, European journal of morphology.

[18]  S. Abraham,et al.  Co‐option of endocytic functions of cellular caveolae by pathogens , 2001, Immunology.

[19]  Dr. Geoffrey R. Newman,et al.  Resin Microscopy and On-Section Immunocytochemistry , 1993, Springer Lab Manuals.

[20]  M. Lisanti,et al.  Caveolae and their coat proteins, the caveolins: from electron microscopic novelty to biological launching pad. , 2001, Journal of cellular physiology.

[21]  D. Hungerford,et al.  Identification of caveolae and detection of caveolin in normal human osteoblasts. , 2001, The Journal of bone and joint surgery. British volume.

[22]  P. Hauschka,et al.  Caveolae in Human and Murine Osteoblasts , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[23]  H. Pass,et al.  Human mesothelial cells are unusually susceptible to simian virus 40-mediated transformation and asbestos cocarcinogenicity. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  H. Yamamoto,et al.  High incidence of SV40-like sequences detection in tumour and peripheral blood cells of Japanese osteosarcoma patients , 2000, British Journal of Cancer.

[25]  O. Devuyst,et al.  Vascular proliferation and enhanced expression of endothelial nitric oxide synthase in human peritoneum exposed to long-term peritoneal dialysis. , 2000, Journal of the American Society of Nephrology : JASN.

[26]  J. Seo,et al.  Caveolin internalization by heat shock or hyperosmotic shock. , 2000, Experimental cell research.

[27]  G. Reifenberger,et al.  Low Frequency of SV40, JC and BK Polyomavirus Sequences in Human Medulloblastomas, Meningiomas and Ependymomas , 2000, Brain pathology.

[28]  H. Zhen,et al.  Expression of the simian virus 40 large tumor antigen (Tag) and formation of Tag‐p53 and Tag‐pRb complexes in human brain tumors , 1999, Cancer.

[29]  J. Engelman,et al.  p42/44 MAP Kinase-dependent and -independent Signaling Pathways Regulate Caveolin-1 Gene Expression , 1999, The Journal of Biological Chemistry.

[30]  J. Coers,et al.  Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth , 1999, Nature Cell Biology.

[31]  H. Pass,et al.  Simian virus 40 (SV40)–like DNA sequences not detectable in Finnish mesothelioma patients not exposed to SV40‐contaminated polio vaccines , 1999, Molecular carcinogenesis.

[32]  J. Hancock,et al.  Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains , 1999, Nature Cell Biology.

[33]  T. Wedel,et al.  Scanning and transmission electron microscopic study of visceral and parietal peritoneal regions in the rat. , 1999, Annals of Anatomy.

[34]  L. Norkin,et al.  Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae. , 1999, Experimental cell research.

[35]  B. Jasani,et al.  Caveolin and its cellular and subcellular immunolocalisation in lung alveolar epithelium: implications for alveolar epithelial type I cell function , 1999, Cell and Tissue Research.

[36]  J. Engelman,et al.  Genes encoding human caveolin‐1 and ‐2 are co‐localized to the D7S522 locus (7q31.1), a known fragile site (FRA7G) that is frequently deleted in human cancers , 1998, FEBS letters.

[37]  G. Goings,et al.  Water channel proteins in rat cardiac myocyte caveolae: osmolarity-dependent reversible internalization. , 1998, American journal of physiology. Heart and circulatory physiology.

[38]  L. Norkin,et al.  MHC class I molecules are enriched in caveolae but do not enter with simian virus 40. , 1998, The Journal of general virology.

[39]  H. Ju,et al.  Interaction of Neuronal Nitric-oxide Synthase with Caveolin-3 in Skeletal Muscle , 1997, The Journal of Biological Chemistry.

[40]  H. Ju,et al.  Direct Interaction of Endothelial Nitric-oxide Synthase and Caveolin-1 Inhibits Synthase Activity* , 1997, The Journal of Biological Chemistry.

[41]  R. Attanoos,et al.  Pathology of malignant mesothelioma , 1997, Histopathology.

[42]  K. Michailova Ultrastructural observations on the human visceral pleura. , 1997, European journal of morphology.

[43]  J. Kartenbeck,et al.  Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. , 1997, Molecular biology of the cell.

[44]  B. Mossman,et al.  Asbestos causes stimulation of the extracellular signal-regulated kinase 1 mitogen-activated protein kinase cascade after phosphorylation of the epidermal growth factor receptor. , 1996, Cancer research.

[45]  C. Fielding,et al.  Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae. , 1996, Biochemistry.

[46]  L. Norkin,et al.  Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. , 1996, Molecular biology of the cell.

[47]  K. Michailova The serous membranes in the cat. Electron microscopic observations. , 1996, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[48]  R. Garcea,et al.  SV40-like sequences in human bone tumors. , 1996, Oncogene.

[49]  X. Chen,et al.  The ultrastructure of vesicle-containing cells and ER-cells of human peritoneum. , 1996, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[50]  K. Carr,et al.  Ultrastructural observations on the peritoneum in the mouse. , 1996, Journal of anatomy.

[51]  R. G. Anderson,et al.  Hormonal regulation of caveolae internalization , 1995, The Journal of cell biology.

[52]  J. Goldblum,et al.  Localized and diffuse mesotheliomas of the genital tract and peritoneum in women. A clinicopathologic study of nineteen true mesothelial neoplasms, other than adenomatoid tumors, multicystic mesotheliomas, and localized fibrous tumors. , 1995, The American journal of surgical pathology.

[53]  Michailova Kn A combined electron microscopic investigation of the peritoneal mesothelium in the rat. , 1995 .

[54]  C. Madhavi,et al.  Light & electron microscopic structure of choroid plexus in hydrocephalic guinea pig. , 1995, The Indian journal of medical research.

[55]  C. Holmes Peritoneal host defense mechanisms in peritoneal dialysis. , 1994, Kidney international. Supplement.

[56]  P. Oh,et al.  Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules , 1994, The Journal of cell biology.

[57]  R. Clark,et al.  Enhanced body growth in uremic rats treated with IGF-I and growth hormone in combination. , 1994, Kidney international.

[58]  H. Pass,et al.  Simian virus 40-like DNA sequences in human pleural mesothelioma. , 1994, Oncogene.

[59]  M. Lucca,et al.  Primary malignant mesothelioma of the pericardium. Case report and literature review. , 1994, Texas Heart Institute journal.

[60]  S. T. Meller,et al.  A scanning and transmission electron microscopic analysis of the cerebral aqueduct in the rabbit , 1993, The Anatomical record.

[61]  G. Goings,et al.  Rat atrial myocyte plasmalemmal caveolae in situ. Reversible experimental increases in caveolar size and in surface density of caveolar necks. , 1993, Circulation research.

[62]  C. Cicala,et al.  SV40 induces mesotheliomas in hamsters. , 1993, The American journal of pathology.

[63]  R. Shalvoy,et al.  Responses of rat pleural mesothelia to increased intrathoracic pressure. , 1993, Experimental lung research.

[64]  D. Soppet,et al.  Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Richard G. W. Anderson,et al.  Caveolin, a protein component of caveolae membrane coats , 1992, Cell.

[66]  R. G. Anderson,et al.  Potocytosis: sequestration and transport of small molecules by caveolae. , 1992, Science.

[67]  J. Ardell,et al.  Regional blood flow to canine parietal pleura and internal intercostal muscle. , 1991, Journal of applied physiology.

[68]  Y. Sasaguri,et al.  Collagenase production by immortalized human aortic endothelial cells infected with simian virus 40 , 1991, Virchows Archiv. B, Cell pathology including molecular pathology.

[69]  A. Raftery,et al.  The ultrastructure of human abdominal mesothelium. , 1989, Journal of anatomy.

[70]  C. Harris,et al.  Establishment of a human in vitro mesothelial cell model system for investigating mechanisms of asbestos-induced mesothelioma. , 1989, The American journal of pathology.

[71]  J. Dobbie Morphology of the peritoneum in CAPD. , 1989, Blood purification.

[72]  H. Misra,et al.  Enteric serosal surface in the piglet. A scanning and transmission electron microscopic study of the mesothelium. , 1987, Journal of submicroscopic cytology.

[73]  J. Dobbie,et al.  The Ultrastructure of the Parietal Peritoneum in Normal and Uremic Man and in Patients on CAPD , 1986 .

[74]  N. Di Paolo,et al.  Morphology of the peritoneal membrane during continuous ambulatory peritoneal dialysis. , 1986, Nephron.

[75]  J. Winchester,et al.  Frontiers in Peritoneal Dialysis , 1986, Springer Berlin Heidelberg.

[76]  Leknes Il Ultrastructure of the parietal pericardium in teleosts. , 1984 .

[77]  P. K. Ray,et al.  Response of ependyma of the rat third ventricle to operative loss of cerebrospinal fluid: a transmission electron microscopical study. , 1984, Journal of anatomy.

[78]  I. L. Leknes Ultrastructure of the parietal pericardium in teleosts. , 1984, Journal of anatomy.

[79]  N. Simionescu,et al.  The Cardiovascular System , 1983 .

[80]  L. Weiss,et al.  Histology : cell and tissue biology , 1983 .

[81]  A. Medline,et al.  Ultrastructure of normal rabbit mesentery. , 1983, Nephron.

[82]  B. Mossman,et al.  The pathogenesis of asbestos-associated diseases. , 1982, The New England journal of medicine.

[83]  J. Dobbie,et al.  Ultrastructural Studies on the Peritoneum with Special Reference to Chronic Ambulatory Peritoneal Dialysis , 1981, Scottish medical journal.

[84]  A. Peters,et al.  The choroid plexus of the mature and aging rat: The choroidal epithelium , 1979, The Anatomical record.

[85]  M. Forbes,et al.  Caveolar systems and sarcoplasmic reticulum in coronary smooth muscle cells of the mouse. , 1979, Journal of ultrastructure research.

[86]  H. Obata,et al.  Differences in normal structure and reaction to adjuvant between the costal and the visceral pleura. , 1978, Archivum histologicum Japonicum = Nihon soshikigaku kiroku.

[87]  M. Bretscher,et al.  Membrane-associated vesicles in fibroblasts , 1977 .

[88]  N. Wang The regional difference of pleural mesothelial cells in rabbits. , 1974, The American review of respiratory disease.

[89]  G. T. Diamandopoulos Leukemia, Lymphoma, and Osteosarcoma Induced in the Syrian Golden Hamster by Simian Virus 40 , 1972, Science.

[90]  C. G. Moertel Peritoneal mesothelioma. , 1972, Gastroenterology.

[91]  J. R. Casley-Smith The dimensions and numbers of small vesicles in cells, endothelial and mesothelial and the significance of these for endothelial permeability * , 1969, Journal of microscopy.

[92]  J. Hope,et al.  OBSERVATIONS ON ULTRASTRUCTURE OF RABBIT MESOTHELIUM. , 1964, Experimental cell research.

[93]  P. Gerber,et al.  SV40-induced ependymomas in newborn hamsters. I. Virus-tumor relationships. , 1962, Virology.

[94]  K. Hama The Fine Structure of the Desmosomes in Frog Mesothelium , 1960, The Journal of biophysical and biochemical cytology.

[95]  E. Yamada THE FINE STRUCTURE OF THE GALL BLADDER EPITHELIUM OF THE MOUSE , 1955, The Journal of biophysical and biochemical cytology.

[96]  D. L. Odor Observations of the rat mesothelium with the electron and phase microscopes. , 1954, The American journal of anatomy.