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Mitochondrial redox studies of oxidative stress in kidneys from diabetic miceSepideh Maleki, Reyhaneh Sepehr, Kevin Staniszewski, Nader Sheibani, Christine M. Sorenson, and Mahsa Ranji »View Author Affiliations
Sepideh Maleki,1
Reyhaneh Sepehr,1
Kevin Staniszewski,1
Nader Sheibani,2
Christine M. Sorenson,3
and Mahsa Ranji1,*
1Biophotonics Laboratory, University of Wisconsin Milwaukee, Department of Electrical Engineering and Computer Science, 3200 N Cramer St., Milwaukee, WI 53211-3029, USA 2Departments of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, 600 Highland Avenue, Madison, WI, 53792-4673, USA 3Department of Pediatrics, University of Wisconsin School of Medicine and Public Health, 600 Highland Avenue, Madison, WI, 53792-4673, USA *Corresponding author: ranji@uwm.edu |
Biomedical Optics Express, Vol. 3, Issue 2, pp. 273-281 (2012)
http://dx.doi.org/10.1364/BOE.3.000273
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Abstract
Chronic hyperglycemia during diabetes leads to increased production of reactive oxygen species (ROS) and increased oxidative stress (OS). Here we investigated whether changes in the metabolic state can be used as a marker of OS progression in kidneys. We examined redox states of kidneys from diabetic mice, Akita/+ and Akita/+;TSP1–/– mice (Akita mice lacking thrombospondin-1, TSP1) with increasing duration of diabetes. OS as measured by mitochondrial redox ratio (NADH/FAD) was detectable shortly after the onset of diabetes and further increased with the duration of diabetes. Thus, cryo fluorescence redox imaging was used as a quantitative marker of OS progression in kidneys from diabetic mice and demonstrated that alterations in the oxidative state of kidneys occur during the early stages of diabetes.
© 2012 OSA
OCIS Codes
(000.1430) General : Biology and medicine
(100.2960) Image processing : Image analysis
(170.0110) Medical optics and biotechnology : Imaging systems
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.6280) Medical optics and biotechnology : Spectroscopy, fluorescence and luminescence
(260.2510) Physical optics : Fluorescence
ToC Category:
Functional Imaging
History
Original Manuscript: November 23, 2011
Revised Manuscript: December 16, 2011
Manuscript Accepted: January 1, 2012
Published: January 10, 2012
Citation
Sepideh Maleki, Reyhaneh Sepehr, Kevin Staniszewski, Nader Sheibani, Christine M. Sorenson, and Mahsa Ranji, "Mitochondrial redox studies of oxidative stress in kidneys from diabetic mice," Biomed. Opt. Express 3, 273-281 (2012)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-3-2-273
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References
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- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
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- B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem.254(11), 4764–4771 (1979). [PubMed]
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- M. D. Breyer, E. Böttinger, F. C. Brosius, T. M. Coffman, R. C. Harris, C. W. Heilig, K. Sharma, and AMDCC, “Mouse models of diabetic nephropathy,” J. Am. Soc. Nephrol.16(1), 27–45 (2005). [CrossRef] [PubMed]
- M. M. Delmastro and J. D. Piganelli, “Oxidative stress and redox modulation potential in type 1 diabetes,” Clin. Dev. Immunol.2011, 593863 (2011). [CrossRef] [PubMed]
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
- I. Giardino, D. Edelstein, and M. Brownlee, “Bcl-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells,” J. Clin. Invest.97(6), 1422–1428 (1996). [CrossRef] [PubMed]
- J. S. Johansen, A. K. Harris, D. J. Rychly, and A. Ergul, “Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice,” Cardiovasc. Diabetol.4(1), 5–9999 (2005). [CrossRef] [PubMed]
- A. Ceriello, S. Kumar, L. Piconi, K. Esposito, and D. Giugliano, “Simultaneous control of hyperglycemia and oxidative stress normalizes endothelial function in type 1 diabetes,” Diabetes Care30(3), 649–654 (2007). [CrossRef] [PubMed]
- J. J. Kelly, J. R. Ewen, S. L. Bernard, R. W. Glenny, and C. H. Barlow, “Regional blood flow measurements from fluorescent microsphere images using an Imaging CryoMicrotome,” Rev. Sci. Instrum.71(1), 228–234 (2000). [CrossRef]
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- S. L. Bernard, J. R. Ewen, C. H. Barlow, J. J. Kelly, S. McKinney, D. A. Frazer, and R. W. Glenny, “High spatial resolution measurements of organ blood flow in small laboratory animals,” Am. J. Physiol. Heart Circ. Physiol.279(5), H2043–H2052 (2000). [PubMed]
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- A. Ceriello, S. Kumar, L. Piconi, K. Esposito, and D. Giugliano, “Simultaneous control of hyperglycemia and oxidative stress normalizes endothelial function in type 1 diabetes,” Diabetes Care30(3), 649–654 (2007). [CrossRef] [PubMed]
- S. L. Bernard, J. R. Ewen, C. H. Barlow, J. J. Kelly, S. McKinney, D. A. Frazer, and R. W. Glenny, “High spatial resolution measurements of organ blood flow in small laboratory animals,” Am. J. Physiol. Heart Circ. Physiol.279(5), H2043–H2052 (2000). [PubMed]
- J. J. Kelly, J. R. Ewen, S. L. Bernard, R. W. Glenny, and C. H. Barlow, “Regional blood flow measurements from fluorescent microsphere images using an Imaging CryoMicrotome,” Rev. Sci. Instrum.71(1), 228–234 (2000). [CrossRef]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- C. M. Sorenson, B. J. Padanilam, and M. R. Hammerman, “Abnormal postpartum renal development and cystogenesis in the bcl-2 (-/-) mouse,” Am. J. Physiol.271(1 Pt 2), F184–F193 (1996). [PubMed]
- J. S. Johansen, A. K. Harris, D. J. Rychly, and A. Ergul, “Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice,” Cardiovasc. Diabetol.4(1), 5–9999 (2005). [CrossRef] [PubMed]
- M. D. Breyer, E. Böttinger, F. C. Brosius, T. M. Coffman, R. C. Harris, C. W. Heilig, K. Sharma, and AMDCC, “Mouse models of diabetic nephropathy,” J. Am. Soc. Nephrol.16(1), 27–45 (2005). [CrossRef] [PubMed]
- M. D. Breyer, E. Böttinger, F. C. Brosius, T. M. Coffman, R. C. Harris, C. W. Heilig, K. Sharma, and AMDCC, “Mouse models of diabetic nephropathy,” J. Am. Soc. Nephrol.16(1), 27–45 (2005). [CrossRef] [PubMed]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- S. S. Chung, E. C. Ho, K. S. Lam, and S. K. Chung, “Contribution of polyol pathway to diabetes-induced oxidative stress,” J. Am. Soc. Nephrol.14(Suppl 3), S233–S236 (2003). [CrossRef] [PubMed]
- N. Susnow, L. Zeng, D. Margineantu, and D. M. Hockenbery, “Bcl-2 family proteins as regulators of oxidative stress,” Semin. Cancer Biol.19(1), 42–49 (2009). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- Q. Huang, S. J. Wang, C. M. Sorenson, and N. Sheibani, “PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxia-mediated vessel obliteration,” Exp. Eye Res.87(3), 226–241 (2008). [CrossRef] [PubMed]
- E. A. Scheef, Q. Huang, S. Wang, C. M. Sorenson, and N. Sheibani, “Isolation and characterization of corneal endothelial cells from wild type and thrombospondin-1 deficient mice,” Mol. Vis.13, 1483–1495 (2007). [PubMed]
- B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem.254(11), 4764–4771 (1979). [PubMed]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- J. S. Johansen, A. K. Harris, D. J. Rychly, and A. Ergul, “Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice,” Cardiovasc. Diabetol.4(1), 5–9999 (2005). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- S. L. Bernard, J. R. Ewen, C. H. Barlow, J. J. Kelly, S. McKinney, D. A. Frazer, and R. W. Glenny, “High spatial resolution measurements of organ blood flow in small laboratory animals,” Am. J. Physiol. Heart Circ. Physiol.279(5), H2043–H2052 (2000). [PubMed]
- J. J. Kelly, J. R. Ewen, S. L. Bernard, R. W. Glenny, and C. H. Barlow, “Regional blood flow measurements from fluorescent microsphere images using an Imaging CryoMicrotome,” Rev. Sci. Instrum.71(1), 228–234 (2000). [CrossRef]
- C. H. Barlow, D. A. Rorvik, and J. J. Kelly, “Imaging epicardial oxygen,” Ann. Biomed. Eng.26(1), 76–85 (1998). [CrossRef] [PubMed]
- G. L. King and M. R. Loeken, “Hyperglycemia-induced oxidative stress in diabetic complications,” Histochem. Cell Biol.122(4), 333–338 (2004). [CrossRef] [PubMed]
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
- A. Ceriello, S. Kumar, L. Piconi, K. Esposito, and D. Giugliano, “Simultaneous control of hyperglycemia and oxidative stress normalizes endothelial function in type 1 diabetes,” Diabetes Care30(3), 649–654 (2007). [CrossRef] [PubMed]
- S. S. Chung, E. C. Ho, K. S. Lam, and S. K. Chung, “Contribution of polyol pathway to diabetes-induced oxidative stress,” J. Am. Soc. Nephrol.14(Suppl 3), S233–S236 (2003). [CrossRef] [PubMed]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- A. K. Zimmermann, F. A. Loucks, E. K. Schroeder, R. J. Bouchard, K. L. Tyler, and D. A. Linseman, “Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria,” J. Biol. Chem.282(40), 29296–29304 (2007). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- G. L. King and M. R. Loeken, “Hyperglycemia-induced oxidative stress in diabetic complications,” Histochem. Cell Biol.122(4), 333–338 (2004). [CrossRef] [PubMed]
- A. K. Zimmermann, F. A. Loucks, E. K. Schroeder, R. J. Bouchard, K. L. Tyler, and D. A. Linseman, “Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria,” J. Biol. Chem.282(40), 29296–29304 (2007). [CrossRef] [PubMed]
- N. Susnow, L. Zeng, D. Margineantu, and D. M. Hockenbery, “Bcl-2 family proteins as regulators of oxidative stress,” Semin. Cancer Biol.19(1), 42–49 (2009). [CrossRef] [PubMed]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- A. Mayevsky, “Brain NADH redox state monitored in vivo by fiber optic surface fluorometry,” Brain Res.319(1), 49–68 (1984). [PubMed]
- S. L. Bernard, J. R. Ewen, C. H. Barlow, J. J. Kelly, S. McKinney, D. A. Frazer, and R. W. Glenny, “High spatial resolution measurements of organ blood flow in small laboratory animals,” Am. J. Physiol. Heart Circ. Physiol.279(5), H2043–H2052 (2000). [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem.254(11), 4764–4771 (1979). [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem.254(11), 4764–4771 (1979). [PubMed]
- C. M. Sorenson, B. J. Padanilam, and M. R. Hammerman, “Abnormal postpartum renal development and cystogenesis in the bcl-2 (-/-) mouse,” Am. J. Physiol.271(1 Pt 2), F184–F193 (1996). [PubMed]
- A. Ceriello, S. Kumar, L. Piconi, K. Esposito, and D. Giugliano, “Simultaneous control of hyperglycemia and oxidative stress normalizes endothelial function in type 1 diabetes,” Diabetes Care30(3), 649–654 (2007). [CrossRef] [PubMed]
- L. Piconi, L. Quagliaro, and A. Ceriello, “Oxidative stress in diabetes,” Clin. Chem. Lab. Med.41(9), 1144–1149 (2003). [CrossRef] [PubMed]
- M. M. Delmastro and J. D. Piganelli, “Oxidative stress and redox modulation potential in type 1 diabetes,” Clin. Dev. Immunol.2011, 593863 (2011). [CrossRef] [PubMed]
- L. Piconi, L. Quagliaro, and A. Ceriello, “Oxidative stress in diabetes,” Clin. Chem. Lab. Med.41(9), 1144–1149 (2003). [CrossRef] [PubMed]
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
- N. Ramanujam, R. Richards-Kortum, S. Thomsen, A. Mahadevan-Jansen, M. Follen, and B. Chance, “Low temperature fluorescence imaging of freeze-trapped human cervical tissues,” Opt. Express8(6), 335–343 (2001). [CrossRef] [PubMed]
- R. Richards-Kortum and E. Sevick-Muraca, “Quantitative optical spectroscopy for tissue diagnosis,” Annu. Rev. Phys. Chem.47(1), 555–606 (1996). [CrossRef] [PubMed]
- C. H. Barlow, D. A. Rorvik, and J. J. Kelly, “Imaging epicardial oxygen,” Ann. Biomed. Eng.26(1), 76–85 (1998). [CrossRef] [PubMed]
- J. S. Johansen, A. K. Harris, D. J. Rychly, and A. Ergul, “Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice,” Cardiovasc. Diabetol.4(1), 5–9999 (2005). [CrossRef] [PubMed]
- E. A. Scheef, C. M. Sorenson, and N. Sheibani, “Attenuation of proliferation and migration of retinal pericytes in the absence of thrombospondin-1,” Am. J. Physiol. Cell Physiol.296(4), C724–C734 (2009). [CrossRef] [PubMed]
- E. A. Scheef, Q. Huang, S. Wang, C. M. Sorenson, and N. Sheibani, “Isolation and characterization of corneal endothelial cells from wild type and thrombospondin-1 deficient mice,” Mol. Vis.13, 1483–1495 (2007). [PubMed]
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
- B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem.254(11), 4764–4771 (1979). [PubMed]
- A. K. Zimmermann, F. A. Loucks, E. K. Schroeder, R. J. Bouchard, K. L. Tyler, and D. A. Linseman, “Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria,” J. Biol. Chem.282(40), 29296–29304 (2007). [CrossRef] [PubMed]
- R. Richards-Kortum and E. Sevick-Muraca, “Quantitative optical spectroscopy for tissue diagnosis,” Annu. Rev. Phys. Chem.47(1), 555–606 (1996). [CrossRef] [PubMed]
- M. D. Breyer, E. Böttinger, F. C. Brosius, T. M. Coffman, R. C. Harris, C. W. Heilig, K. Sharma, and AMDCC, “Mouse models of diabetic nephropathy,” J. Am. Soc. Nephrol.16(1), 27–45 (2005). [CrossRef] [PubMed]
- E. A. Scheef, C. M. Sorenson, and N. Sheibani, “Attenuation of proliferation and migration of retinal pericytes in the absence of thrombospondin-1,” Am. J. Physiol. Cell Physiol.296(4), C724–C734 (2009). [CrossRef] [PubMed]
- Q. Huang, S. J. Wang, C. M. Sorenson, and N. Sheibani, “PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxia-mediated vessel obliteration,” Exp. Eye Res.87(3), 226–241 (2008). [CrossRef] [PubMed]
- E. A. Scheef, Q. Huang, S. Wang, C. M. Sorenson, and N. Sheibani, “Isolation and characterization of corneal endothelial cells from wild type and thrombospondin-1 deficient mice,” Mol. Vis.13, 1483–1495 (2007). [PubMed]
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
- W. I. Sivitz and M. A. Yorek, “Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities,” Antioxid. Redox Signal.12(4), 537–577 (2010). [CrossRef] [PubMed]
- E. A. Scheef, C. M. Sorenson, and N. Sheibani, “Attenuation of proliferation and migration of retinal pericytes in the absence of thrombospondin-1,” Am. J. Physiol. Cell Physiol.296(4), C724–C734 (2009). [CrossRef] [PubMed]
- Q. Huang, S. J. Wang, C. M. Sorenson, and N. Sheibani, “PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxia-mediated vessel obliteration,” Exp. Eye Res.87(3), 226–241 (2008). [CrossRef] [PubMed]
- E. A. Scheef, Q. Huang, S. Wang, C. M. Sorenson, and N. Sheibani, “Isolation and characterization of corneal endothelial cells from wild type and thrombospondin-1 deficient mice,” Mol. Vis.13, 1483–1495 (2007). [PubMed]
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
- C. M. Sorenson, B. J. Padanilam, and M. R. Hammerman, “Abnormal postpartum renal development and cystogenesis in the bcl-2 (-/-) mouse,” Am. J. Physiol.271(1 Pt 2), F184–F193 (1996). [PubMed]
- G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol.68(5), 603–632 (1998). [PubMed]
- N. Susnow, L. Zeng, D. Margineantu, and D. M. Hockenbery, “Bcl-2 family proteins as regulators of oxidative stress,” Semin. Cancer Biol.19(1), 42–49 (2009). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- A. K. Zimmermann, F. A. Loucks, E. K. Schroeder, R. J. Bouchard, K. L. Tyler, and D. A. Linseman, “Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria,” J. Biol. Chem.282(40), 29296–29304 (2007). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
- G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol.68(5), 603–632 (1998). [PubMed]
- E. A. Scheef, Q. Huang, S. Wang, C. M. Sorenson, and N. Sheibani, “Isolation and characterization of corneal endothelial cells from wild type and thrombospondin-1 deficient mice,” Mol. Vis.13, 1483–1495 (2007). [PubMed]
- Q. Huang, S. J. Wang, C. M. Sorenson, and N. Sheibani, “PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxia-mediated vessel obliteration,” Exp. Eye Res.87(3), 226–241 (2008). [CrossRef] [PubMed]
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- B. Chance and G. R. Williams, “A method for the localization of sites for oxidative phosphorylation,” Nature176(4475), 250–254 (1955). [CrossRef] [PubMed]
- G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol.68(5), 603–632 (1998). [PubMed]
- W. I. Sivitz and M. A. Yorek, “Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities,” Antioxid. Redox Signal.12(4), 537–577 (2010). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
- N. Susnow, L. Zeng, D. Margineantu, and D. M. Hockenbery, “Bcl-2 family proteins as regulators of oxidative stress,” Semin. Cancer Biol.19(1), 42–49 (2009). [CrossRef] [PubMed]
- A. K. Zimmermann, F. A. Loucks, E. K. Schroeder, R. J. Bouchard, K. L. Tyler, and D. A. Linseman, “Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria,” J. Biol. Chem.282(40), 29296–29304 (2007). [CrossRef] [PubMed]
Am. J. Physiol.
- C. M. Sorenson, B. J. Padanilam, and M. R. Hammerman, “Abnormal postpartum renal development and cystogenesis in the bcl-2 (-/-) mouse,” Am. J. Physiol.271(1 Pt 2), F184–F193 (1996). [PubMed]
Am. J. Physiol. Cell Physiol.
- E. A. Scheef, C. M. Sorenson, and N. Sheibani, “Attenuation of proliferation and migration of retinal pericytes in the absence of thrombospondin-1,” Am. J. Physiol. Cell Physiol.296(4), C724–C734 (2009). [CrossRef] [PubMed]
Am. J. Physiol. Heart Circ. Physiol.
- S. L. Bernard, J. R. Ewen, C. H. Barlow, J. J. Kelly, S. McKinney, D. A. Frazer, and R. W. Glenny, “High spatial resolution measurements of organ blood flow in small laboratory animals,” Am. J. Physiol. Heart Circ. Physiol.279(5), H2043–H2052 (2000). [PubMed]
Ann. Biomed. Eng.
- C. H. Barlow, D. A. Rorvik, and J. J. Kelly, “Imaging epicardial oxygen,” Ann. Biomed. Eng.26(1), 76–85 (1998). [CrossRef] [PubMed]
Annu. Rev. Phys. Chem.
- R. Richards-Kortum and E. Sevick-Muraca, “Quantitative optical spectroscopy for tissue diagnosis,” Annu. Rev. Phys. Chem.47(1), 555–606 (1996). [CrossRef] [PubMed]
Antioxid. Redox Signal.
- W. I. Sivitz and M. A. Yorek, “Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities,” Antioxid. Redox Signal.12(4), 537–577 (2010). [CrossRef] [PubMed]
Biosci. Biotechnol. Biochem.
- Y. Ueno, F. Horio, K. Uchida, M. Naito, H. Nomura, Y. Kato, T. Tsuda, S. Toyokuni, and T. Osawa, “Increase in oxidative stress in kidneys of diabetic Akita mice,” Biosci. Biotechnol. Biochem.66(4), 869–872 (2002). [CrossRef] [PubMed]
Brain Res.
- A. Mayevsky, “Brain NADH redox state monitored in vivo by fiber optic surface fluorometry,” Brain Res.319(1), 49–68 (1984). [PubMed]
Cardiovasc. Diabetol.
- J. S. Johansen, A. K. Harris, D. J. Rychly, and A. Ergul, “Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice,” Cardiovasc. Diabetol.4(1), 5–9999 (2005). [CrossRef] [PubMed]
Clin. Chem. Lab. Med.
- L. Piconi, L. Quagliaro, and A. Ceriello, “Oxidative stress in diabetes,” Clin. Chem. Lab. Med.41(9), 1144–1149 (2003). [CrossRef] [PubMed]
Clin. Dev. Immunol.
- M. M. Delmastro and J. D. Piganelli, “Oxidative stress and redox modulation potential in type 1 diabetes,” Clin. Dev. Immunol.2011, 593863 (2011). [CrossRef] [PubMed]
Diabetes
- H. Bugger, S. Boudina, X. X. Hu, J. Tuinei, V. G. Zaha, H. A. Theobald, U. J. Yun, A. P. McQueen, B. Wayment, S. E. Litwin, and E. D. Abel, “Type 1 diabetic Akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3,” Diabetes57(11), 2924–2932 (2008). [CrossRef] [PubMed]
Diabetes Care
- A. Ceriello, S. Kumar, L. Piconi, K. Esposito, and D. Giugliano, “Simultaneous control of hyperglycemia and oxidative stress normalizes endothelial function in type 1 diabetes,” Diabetes Care30(3), 649–654 (2007). [CrossRef] [PubMed]
Exp. Eye Res.
- Q. Huang, S. J. Wang, C. M. Sorenson, and N. Sheibani, “PEDF-deficient mice exhibit an enhanced rate of retinal vascular expansion and are more sensitive to hyperoxia-mediated vessel obliteration,” Exp. Eye Res.87(3), 226–241 (2008). [CrossRef] [PubMed]
Histochem. Cell Biol.
- G. L. King and M. R. Loeken, “Hyperglycemia-induced oxidative stress in diabetic complications,” Histochem. Cell Biol.122(4), 333–338 (2004). [CrossRef] [PubMed]
IEEE Trans. Biomed. Eng.
- M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, and J. H. Gorman, “Quantifying acute myocardial injury using ratiometric fluorometry,” IEEE Trans. Biomed. Eng.56(5), 1556–1563 (2009). [CrossRef] [PubMed]
J. Am. Soc. Nephrol.
- S. S. Chung, E. C. Ho, K. S. Lam, and S. K. Chung, “Contribution of polyol pathway to diabetes-induced oxidative stress,” J. Am. Soc. Nephrol.14(Suppl 3), S233–S236 (2003). [CrossRef] [PubMed]
- M. D. Breyer, E. Böttinger, F. C. Brosius, T. M. Coffman, R. C. Harris, C. W. Heilig, K. Sharma, and AMDCC, “Mouse models of diabetic nephropathy,” J. Am. Soc. Nephrol.16(1), 27–45 (2005). [CrossRef] [PubMed]
J. Biol. Chem.
- B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem.254(11), 4764–4771 (1979). [PubMed]
- A. K. Zimmermann, F. A. Loucks, E. K. Schroeder, R. J. Bouchard, K. L. Tyler, and D. A. Linseman, “Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria,” J. Biol. Chem.282(40), 29296–29304 (2007). [CrossRef] [PubMed]
J. Biomed. Opt.
- M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, R. C. Gorman, D. L. Jaggard, and B. Chance, “Fluorescence spectroscopy and imaging of myocardial apoptosis,” J. Biomed. Opt.11(6), 064036 (2006). [CrossRef] [PubMed]
J. Cell. Physiol.
- N. Sheibani, E. A. Scheef, T. A. Dimaio, Y. Wang, S. Kondo, and C. M. Sorenson, “Bcl-2 expression modulates cell adhesion and migration promoting branching of ureteric bud cells,” J. Cell. Physiol.210(3), 616–625 (2007). [CrossRef] [PubMed]
J. Clin. Invest.
- I. Giardino, D. Edelstein, and M. Brownlee, “Bcl-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells,” J. Clin. Invest.97(6), 1422–1428 (1996). [CrossRef] [PubMed]
Mol. Vis.
- E. A. Scheef, Q. Huang, S. Wang, C. M. Sorenson, and N. Sheibani, “Isolation and characterization of corneal endothelial cells from wild type and thrombospondin-1 deficient mice,” Mol. Vis.13, 1483–1495 (2007). [PubMed]
Nature
- B. Chance and G. R. Williams, “A method for the localization of sites for oxidative phosphorylation,” Nature176(4475), 250–254 (1955). [CrossRef] [PubMed]
Opt. Express
- N. Ramanujam, R. Richards-Kortum, S. Thomsen, A. Mahadevan-Jansen, M. Follen, and B. Chance, “Low temperature fluorescence imaging of freeze-trapped human cervical tissues,” Opt. Express8(6), 335–343 (2001). [CrossRef] [PubMed]
Photochem. Photobiol.
- G. A. Wagnières, W. M. Star, and B. C. Wilson, “In vivo fluorescence spectroscopy and imaging for oncological applications,” Photochem. Photobiol.68(5), 603–632 (1998). [PubMed]
Rev. Sci. Instrum.
- J. J. Kelly, J. R. Ewen, S. L. Bernard, R. W. Glenny, and C. H. Barlow, “Regional blood flow measurements from fluorescent microsphere images using an Imaging CryoMicrotome,” Rev. Sci. Instrum.71(1), 228–234 (2000). [CrossRef]
Semin. Cancer Biol.
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