Abstract

A detailed microscopic analysis of renal podocyte substructure is essential to understand and diagnose nephrotic kidney disease. Currently only time consuming electron microscopy (EM) can resolve this substructure. We used structured illumination microscopy (SIM) to examine frozen sections of renal biopsies stained with an immunofluorescence marker for podocin, a protein localized to the perimeter of the podocyte foot processes and compared them with EM in both normal and nephrotic disease biopsies. SIM images of normal glomeruli revealed curvilinear patterns of podocin densely covering capillary walls similar to podocyte foot processes seen by EM. Podocin staining of all nephrotic disease biopsies were significantly different than normal, corresponding to and better visualizing effaced foot processes seen by EM. The findings support the first potential use of SIM in the diagnosis of nephrotic disease.

© 2016 Optical Society of America

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References

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2015 (1)

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

2014 (1)

2013 (2)

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

2012 (1)

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

2010 (1)

P. Mundel and J. Reiser, “Proteinuria: an enzymatic disease of the podocyte?” Kidney Int. 77(7), 571–580 (2010).
[Crossref] [PubMed]

2008 (2)

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

2002 (1)

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

2000 (1)

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

1997 (1)

1980 (1)

H. J. G. Gundersen, T. Seefeldt, and R. Østerby, “Glomerular epithelial foot processes in normal man and rats. distribution of true width and its intra- and inter-individual variation,” Cell Tissue Res. 205(1), 147–155 (1980).
[Crossref] [PubMed]

1974 (1)

R. Rodewald and M. J. Karnovsky, “Porous substructure of the glomerular slit diaphragm in the rat and mouse,” J. Cell Biol. 60(2), 423–433 (1974).
[Crossref] [PubMed]

1971 (1)

M. Arakawa, “A Scanning Electron Microscope Study of the Human Glomerulus,” Am. J. Pathol. 64(2), 457–466 (1971).
[PubMed]

Agard, D. A.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Antignac, C.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Arakawa, M.

M. Arakawa, “A Scanning Electron Microscope Study of the Human Glomerulus,” Am. J. Pathol. 64(2), 457–466 (1971).
[PubMed]

Attié, T.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Baird, M. A.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Beach, J. R.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Benessy, F.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Benzing, T.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Betzig, E.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Bijol, V.

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

Blom, H.

D. Unnersjö-Jess, L. Scott, H. Blom, and H. Brismar, “Super-resolution stimulated emission depletion imaging of slit diaphragm proteins in optically cleared kidney tissue,” Kidney Int. (2015), doi:.
[Crossref]

Bonventre, J. V.

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

Borm, G. F.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Boute, N.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Brähler, S.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Brinkkoetter, P. T.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Brismar, H.

D. Unnersjö-Jess, L. Scott, H. Blom, and H. Brismar, “Super-resolution stimulated emission depletion imaging of slit diaphragm proteins in optically cleared kidney tissue,” Kidney Int. (2015), doi:.
[Crossref]

Brooks, C. R.

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

Brown, J. Q.

Campbell, E. C.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

Cande, W. Z.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Carlton, P. M.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Chen, B.-C.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Dani, A.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Davidson, M. W.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Deegens, J. K.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Dholakia, K.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

Dijkman, H. B.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Elfer, K. N.

Golubovskaya, I. N.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Grgic, I.

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

Gribouval, O.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Gubler, M.-C.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Gundersen, H. J. G.

H. J. G. Gundersen, T. Seefeldt, and R. Østerby, “Glomerular epithelial foot processes in normal man and rats. distribution of true width and its intra- and inter-individual variation,” Cell Tissue Res. 205(1), 147–155 (1980).
[Crossref] [PubMed]

Gunn-Moore, F. J.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

Gustafsson, M. G. L.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

Hagmann, H.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Hammer, J. A.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Heuser, J. E.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Hofmeister, A. F.

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

Höhne, M.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Humphreys, B. D.

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

Ising, C.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Juškaitis, R.

Karnovsky, M. J.

R. Rodewald and M. J. Karnovsky, “Porous substructure of the glomerular slit diaphragm in the rat and mouse,” J. Cell Biol. 60(2), 423–433 (1974).
[Crossref] [PubMed]

Kirchhausen, T.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Li, D.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Milkie, D. E.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Miner, J. H.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Moses, B.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Mundel, P.

P. Mundel and J. Reiser, “Proteinuria: an enzymatic disease of the podocyte?” Kidney Int. 77(7), 571–580 (2010).
[Crossref] [PubMed]

Neil, M. A. A.

Nylk, J.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

Østerby, R.

H. J. G. Gundersen, T. Seefeldt, and R. Østerby, “Glomerular epithelial foot processes in normal man and rats. distribution of true width and its intra- and inter-individual variation,” Cell Tissue Res. 205(1), 147–155 (1980).
[Crossref] [PubMed]

Pasham, M.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Prystowsky, M. B.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

Pullman, J.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

Reiser, J.

P. Mundel and J. Reiser, “Proteinuria: an enzymatic disease of the podocyte?” Kidney Int. 77(7), 571–580 (2010).
[Crossref] [PubMed]

Rodewald, R.

R. Rodewald and M. J. Karnovsky, “Porous substructure of the glomerular slit diaphragm in the rat and mouse,” J. Cell Biol. 60(2), 423–433 (1974).
[Crossref] [PubMed]

Roselli, S.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Roth, R.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Schermer, B.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Schlichenmeyer, T. C.

Scott, L.

D. Unnersjö-Jess, L. Scott, H. Blom, and H. Brismar, “Super-resolution stimulated emission depletion imaging of slit diaphragm proteins in optically cleared kidney tissue,” Kidney Int. (2015), doi:.
[Crossref]

Sedat, J. W.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Seefeldt, T.

H. J. G. Gundersen, T. Seefeldt, and R. Østerby, “Glomerular epithelial foot processes in normal man and rats. distribution of true width and its intra- and inter-individual variation,” Cell Tissue Res. 205(1), 147–155 (1980).
[Crossref] [PubMed]

Shao, L.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Shaw, A. S.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Sich, M.

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

Steenbergen, E. J.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Suleiman, H.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Unnersjö-Jess, D.

D. Unnersjö-Jess, L. Scott, H. Blom, and H. Brismar, “Super-resolution stimulated emission depletion imaging of slit diaphragm proteins in optically cleared kidney tissue,” Kidney Int. (2015), doi:.
[Crossref]

van den Berg, J. G.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Völker, L. A.

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

Wang, C. J. R.

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Wang, M.

Weening, J. J.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Wetzels, J. F.

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

Wilson, T.

Xu, P.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Zhang, L.

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

Zhang, M.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Zhang, X.

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Am. J. Pathol. (3)

M. Höhne, C. Ising, H. Hagmann, L. A. Völker, S. Brähler, B. Schermer, P. T. Brinkkoetter, and T. Benzing, “Light microscopic visualization of podocyte ultrastructure demonstrates oscillating glomerular contractions,” Am. J. Pathol. 182(2), 332–338 (2013).
[Crossref] [PubMed]

S. Roselli, O. Gribouval, N. Boute, M. Sich, F. Benessy, T. Attié, M.-C. Gubler, and C. Antignac, “Podocin Localizes in the Kidney to the Slit Diaphragm Area,” Am. J. Pathol. 160(1), 131–139 (2002).
[Crossref] [PubMed]

M. Arakawa, “A Scanning Electron Microscope Study of the Human Glomerulus,” Am. J. Pathol. 64(2), 457–466 (1971).
[PubMed]

Biomed. Opt. Express (1)

Biophys. J. (1)

M. G. L. Gustafsson, L. Shao, P. M. Carlton, C. J. R. Wang, I. N. Golubovskaya, W. Z. Cande, D. A. Agard, and J. W. Sedat, “Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination,” Biophys. J. 94(12), 4957–4970 (2008).
[Crossref] [PubMed]

Cell Tissue Res. (1)

H. J. G. Gundersen, T. Seefeldt, and R. Østerby, “Glomerular epithelial foot processes in normal man and rats. distribution of true width and its intra- and inter-individual variation,” Cell Tissue Res. 205(1), 147–155 (1980).
[Crossref] [PubMed]

eLife (1)

H. Suleiman, L. Zhang, R. Roth, J. E. Heuser, J. H. Miner, A. S. Shaw, and A. Dani, “Nanoscale protein architecture of the kidney glomerular basement membrane,” eLife 2, e01149 (2013).
[PubMed]

J. Am. Soc. Nephrol. (1)

I. Grgic, C. R. Brooks, A. F. Hofmeister, V. Bijol, J. V. Bonventre, and B. D. Humphreys, “Imaging of podocyte foot processes by fluorescence microscopy,” J. Am. Soc. Nephrol. 23(5), 785–791 (2012).
[Crossref] [PubMed]

J. Cell Biol. (1)

R. Rodewald and M. J. Karnovsky, “Porous substructure of the glomerular slit diaphragm in the rat and mouse,” J. Cell Biol. 60(2), 423–433 (1974).
[Crossref] [PubMed]

J. Microsc. (1)

M. G. L. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref] [PubMed]

Kidney Int. (2)

J. K. Deegens, H. B. Dijkman, G. F. Borm, E. J. Steenbergen, J. G. van den Berg, J. J. Weening, and J. F. Wetzels, “Podocyte foot process effacement as a diagnostic tool in focal segmental glomerulosclerosis,” Kidney Int. 74(12), 1568–1576 (2008).
[Crossref] [PubMed]

P. Mundel and J. Reiser, “Proteinuria: an enzymatic disease of the podocyte?” Kidney Int. 77(7), 571–580 (2010).
[Crossref] [PubMed]

Opt. Lett. (1)

Science (1)

D. Li, L. Shao, B.-C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref] [PubMed]

Other (3)

J. J. Bozzola and L. D. Russel, Electron Microscopy: Principles and Techniques for Biologists, 2nd ed. (Jones and Bartlett Publishers, c1999), Chap. 2.

J. Pullman, J. Nylk, E. C. Campbell, F. J. Gunn-Moore, M. B. Prystowsky, and K. Dholakia, “Data underpinning: Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease”.

D. Unnersjö-Jess, L. Scott, H. Blom, and H. Brismar, “Super-resolution stimulated emission depletion imaging of slit diaphragm proteins in optically cleared kidney tissue,” Kidney Int. (2015), doi:.
[Crossref]

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Figures (5)

Fig. 1
Fig. 1 Normal (a, b, c, e, f) and nephrotic (d, g, h) glomerular podocyte substructure. P = pedicel, FP = foot process, CB = cell body, MP = major pedicel processes, SD = slit diaphragm, GBM = glomerular basement membrane. (a) Representation of the glomerulus with podocyte cell bodies wrapping around capillaries, (b) higher magnification view of (a) showing the highly interdigitated structure of pedicels and foot processes, (c) SEM view similar to (b). (d) SEM view of altered podocyte substructure in nephrotic syndrome, (e) cross sectional view by TEM of podocyte foot processes (FP) against the GBM, (f) schematic en face view of normal podocyte foot processes, (g) TEM image of a nephrotic podocyte without visible foot processes, (h) schematic en face view of nephrotic podocytes. (a-b) reprinted from Wikipedia commons, (c-h) from reference [1] with permission from Macmillan Publishers, Ltd.
Fig. 2
Fig. 2 Epi-fluorescence imaging of a FITC-podocin stained normal glomerulus. (a) Section of a whole glomerulus at 20x magnification showing the outlines of many interconnected capillaries. (b) High magnification (100x) image of the region outlined by the white square in (a), showing cross sections (X) and some partial en face views (E) of capillaries as they curve through the section. Squares with (L) denote the capillary lumens. The data set can be accessed at [15].
Fig. 3
Fig. 3 3D-SIM imaging of a FITC-podocin stained normal glomerulus. Maximum intensity projection of a SIM z-stack (79 planes, 9.36μm thick) at 100x. (a) Same region as shown in Fig. 2(b). Squares with (L) denote the capillary lumens. Image shows cross sectional and en face views of podocytes foot processes as they curve around capillary walls. Arrows point to well-resolved podocyte outlines. (b) and (d) Enlargements of two areas marked with arrows in (a). FP = foot process, P = pedicel. (c) and (e) EM sections with similar en face views of podocytes at the same magnification as (b) and (d). The data set can be accessed at [15].
Fig. 4
Fig. 4 Epi-fluorescence imaging of a FITC-podocin stained glomerulus from a patient with nephrotic syndrome (minimal change disease). (a) Section of a whole glomerulus at 20x magnification showing the outlines of many interconnected capillaries, identical in appearance to those in the normal glomerulus in Fig. 2(a). (b) High magnification (100x) image of the region outlined by the white square in (a), showing a cross section (X) and an en face view (E) of one capillary curving through the section. Square with (L) denotes the capillary lumen. The data set can be accessed at [15].
Fig. 5
Fig. 5 3D-SIM image of a FITC-podocin stained glomerular capillary from a patient with nephrotic syndrome (minimal change disease). Maximum intensity projection of a SIM z-stack (100x; 67 planes, 7.92μm thick). Foot processes (FP) appear variably enlarged and sparser than the normal ones in Fig. 3. Straight or minimally curved lines (SL) represent completely effaced foot processes. Square with (L) denotes the capillary lumen. The data set can be accessed at [15].

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