High glucose repatterns human podocyte energy metabolism during differentiation and diabetic nephropathy

FASEB Journal

Volumn 31, Issue 1, 2017, Pages 294-307

  Imasawa, Toshiyuki ^a   Obre, Emilie ^b,c   Bellance, Nadège ^b   Lavie, Julie ^b   Imasawa, Tomoko ^b   Rigothier, Claire ^d   Delmas, Yahsou ^d   Combe, Christian ^d   Lacombe, Didier ^b   Benard, Giovanni ^b   Claverol, Stéphane ^b   Bonneu, Marc ^b   Rossignol, Rodrigue ^b,c  

^a SAKURA NATIONAL HOSPITAL   (Japan)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c HÔPITAL PELLEGRIN   (France)

^d BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

Human kidney; MEF2C; Mitochondria

Indexed keywords

GLUCOSE; GLYCOLYTIC ENZYME; MYOCYTE ENHANCER FACTOR 2; MYOGENIC FACTOR 5; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN SERINE THREONINE KINASE; SERINE THREONINE LIVER KINASE B1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ARTICLE; BIOGENESIS; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENERGY METABOLISM; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRACELLULAR SIGNALING; KIDNEY TISSUE; LACTIC ACIDOSIS; MITOCHONDRIAL BIOGENESIS; OXIDATIVE PHOSPHORYLATION; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE SECTION; BOWMAN CAPSULE; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; PHYSIOLOGY;

BOWMAN CAPSULE; CELL DIFFERENTIATION; CELLS, CULTURED; DIABETIC NEPHROPATHIES; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; OXIDATION-REDUCTION; PODOCYTES;

EID: 85009804125     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201600293R     Document Type: Article

References (55)

1. Dronavalli, S., Duka, I., and Bakris, G. L. (2008) The pathogenesis of diabetic nephropathy. Nat. Clin. Pract. Endocrinol. Metab. 4, 444-452
2. Gassler, N., Elger, M., Kränzlin, B., Kriz, W., Gretz, N., Hähnel, B., Hosser, H., and Hartmann, I. (2001) Podocyte injury underlies the progressionof focal segmental glomerulosclerosis in the fa/faZucker rat. Kidney Int. 60, 106-116
3. Hara, M., Yamagata, K., Tomino, Y., Saito, A., Hirayama, Y., Ogasawara, S., Kurosawa, H., Sekine, S., and Yan, K. (2012) Urinary podocalyxin is an early marker for podocyte injury in patients with diabetes: establishment of a highly sensitive ELISA to detect urinary podocalyxin. Diabetologia 55, 2913-2919
4. Li, J. J., Kwak, S. J., Jung, D. S., Kim, J. J., Yoo, T. H., Ryu, D. R., Han, S. H., Choi, H. Y., Lee, J. E., Moon, S. J., Kim, D. K., Han, D. S., and Kang, S.W. (2007) Podocyte biology in diabetic nephropathy. Kidney Int. Suppl. 72(106), S36-S42
5. Ihalmo, P., Wessman, M., Kaunisto, M. A., Kilpikari, R., Parkkonen, M., Forsblom, C., Holthöfer, H., and Groop, P. H.; FinnDiane Study Group. (2008) Association analysis of podocyte slit diaphragm genes as candidates for diabetic nephropathy. Diabetologia 51, 86-90
6. Imasawa, T., and Rossignol, R. (2013) Podocyte energy metabolism and glomerular diseases. Int. J. Biochem. Cell Biol. 45, 2109-2118
7. Abe, Y., Sakairi, T., Kajiyama, H., Shrivastav, S., Beeson, C., andKopp, J. B. (2010) Bioenergetic characterization ofmouse podocytes. Am. J. Physiol. Cell Physiol. 299, C464-C476
8. Güçer, S., Talim, B., Asçan, E., Korkusuz, P., Ozen, S., Unal, S., Kalkanoǧlu, S. H., Kale, G., and Caǧlar, M. (2005) Focal segmental glomerulosclerosis associatedwithmitochondrial cytopathy: report of two cases with special emphasis on podocytes. Pediatr. Dev. Pathol. 8, 710-717
9. Diomedi-Camassei, F., DiGiandomenico, S., Santorelli, F. M., Caridi, G., Piemonte, F., Montini, G., Ghiggeri, G. M., Murer, L., Barisoni, L., Pastore, A., Muda, A.O., Valente, M.L., Bertini, E., andEmma, F.(2007) COQ2 nephropathy: a newly described inherited mitochondriopathy with primary renal involvement. J. Am. Soc. Nephrol. 18, 2773-2780
10. Stieger, N., Worthmann, K., Teng, B., Engeli, S., Das, A.M., Haller, H., and Schiffer, M. (2012) Impact of high glucose and transforming growth factor-b on bioenergetic profiles in podocytes. Metabolism 61, 1073-1086
11. Sharma, K., Karl, B., Mathew, A. V., Gangoiti, J.A., Wassel, C. L., Saito, R., Pu, M., Sharma, S., You, Y. H., Wang, L., Diamond-Stanic, M., Lindenmeyer, M. T., Forsblom, C., Wu, W., Ix, J.H., Ideker, T., Kopp, J. B., Nigam, S. K., Cohen, C. D., Groop, P. H., Barshop, B. A., Natarajan, L., Nyhan, W.L., andNaviaux, R. K. (2013)Metabolomics reveals signature of mitochondrial dysfunction in diabetic kidney disease. J. Am. Soc. Nephrol. 24, 1901-1912
12. Ahmed, M., Muhammed, S. J., Kessler, B., and Salehi, A. (2010) Mitochondrial proteome analysis reveals alteredexpressionof voltage dependent anion channels in pancreatic b-cells exposed to high glucose. Islets 2, 283-292
13. Mootha, V. K., Lindgren, C. M., Eriksson, K. F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E., Houstis, N., Daly, M. J., Patterson, N., Mesirov, J. P., Golub, T. R., Tamayo, P., Spiegelman, B., Lander, E. S., Hirschhorn, J. N., Altshuler, D., and Groop, L. C. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267-273
14. Gao, C. L., Zhu, C., Zhao, Y. P., Chen, X. H., Ji, C. B., Zhang, C. M., Zhu, J. G., Xia, Z. K., Tong, M. L., and Guo, X. R. (2010) Mitochondrial dysfunction is induced by high levels of glucose and free fatty acids in 3T3-L1 adipocytes. Mol. Cell. Endocrinol. 320, 25-33
15. Leinninger, G. M., Edwards, J. L., Lipshaw, M. J., and Feldman, E. L. (2006) Mechanisms of disease: mitochondria as new therapeutic targets in diabetic neuropathy. Nat. Clin. Pract. Neurol. 2, 620-628
16. Russell, N. D., and Cooper, M. E. (2015) 50 years forward: mechanisms of hyperglycaemia-driven diabetic complications. Diabetologia 58, 1708-1714
17. May, C. J., Saleem, M., andWelsh, G. I.(2014)Podocytededifferentiation: a specialized process for a specialized cell. Front. Endocrinol. (Lausanne) 5, 148
18. Li, S. Y., Huang, P.H., Yang, A.H., Tarng, D.C., Yang, W.C., Lin, C.C., Chen, J. W., Schmid-Schönbein, G., and Lin, S. J. (2014) Matrix metalloproteinase-9 deficiency attenuates diabetic nephropathy by modulation of podocyte functions and dedifferentiation. Kidney Int. 86, 358-369
19. Saleem, M. A., O'Hare, M. J., Reiser, J., Coward, R. J., Inward, C. D., Farren, T., Xing, C. Y., Ni, L., Mathieson, P.W., andMundel, P. (2002)A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J. Am. Soc. Nephrol. 13, 630-638
20. Rigothier, C., Auguste, P., Welsh, G. I., Lepreux, S., Deminíere, C., Mathieson, P. W., Saleem, M. A., Ripoche, J., and Combe, C. (2012) IQGAP1 interacts with components of the slit diaphragmcomplex in podocytes and is involved in podocyte migration and permeability in vitro. PLoS One 7, e37695
21. Benard, G., Bellance, N., James, D., Parrone, P., Fernandez, H., Letellier, T., and Rossignol, R. (2007) Mitochondrial bioenergetics and structural network organization. J. Cell Sci. 120, 838-848
22. Melser, S., Chatelain, E. H., Lavie, J., Mahfouf, W., Jose, C., Obre, E., Goorden, S., Priault, M., Elgersma, Y., Rezvani, H. R., Rossignol, R., and Bénard, G. (2013) Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab. 17, 719-730
23. Medja, F., Allouche, S., Frachon, P., Jardel, C., Malgat, M., Mousson de Camaret, B., Slama, A., Lunardi, J., Mazat, J. P., and Lombés, A. (2009) Development andimplementation of standardized respiratory chain spectrophotometric assays for clinical diagnosis. Mitochondrion 9, 331-339
24. Fessart, D., Martin-Negrier, M. L., Claverol, S., Thiolat, M. L., Crevel, H., Toussaint, C., Bonneu, M., Muller, B., Savineau, J. P., and Delom, F. (2014) Proteomic remodeling of proteasome in right heart failure. J. Mol. Cell. Cardiol. 66, 41-52
25. Velpula, K. K., Bhasin, A., Asuthkar, S., and Tsung, A. J. (2013) Combined targeting of PDK1 and EGFR triggers regression of glioblastoma by reversing the Warburg effect. Cancer Res. 73, 7277-7289
26. Czubryt, M. P., McAnally, J., Fishman, G. I., and Olson, E. N. (2003) Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc. Natl. Acad. Sci. USA 100, 1711-1716
27. Johanson, M., Meents, H., Ragge, K., Buchberger, A., Arnold, H. H., and Sandmöller, A. (1999) Transcriptional activation of the myogenin gene by MEF2-mediated recruitment of myf5 is inhibited by adenovirus E1A protein. Biochem. Biophys. Res. Commun. 265, 222-232
28. Yang, L., Xie, M., Yang, M., Yu, Y., Zhu, S., Hou, W., Kang, R., Lotze, M. T., Billiar, T. R., Wang, H., Cao, L., and Tang, D. (2014) PKM2 regulates theWarburg effect and promotesHMGB1 release in sepsis. Nat. Commun. 5, 4436
29. Emma, F., Montini, G., Parikh, S. M., and Salviati, L. (2016) Mitochondrial dysfunction in inherited renal disease and acute kidney injury. Nat. Rev. Nephrol. 12, 267-280
30. Reidy, K., Kang, H.M., Hostetter, T., andSusztak, K. (2014)Molecular mechanisms of diabetic kidney disease. J. Clin. Invest. 124, 2333-2340
31. Cheval, L., Pierrat, F., Rajerison, R., Piquemal, D., and Doucet, A. (2012) Of mice and men: divergence of gene expression patterns in kidney. PLoS One 7, e46876
32. O'Brien, L.L., Guo, Q., Lee, Y., Tran, T., Benazet, J.D., Whitney, P.H., Valouev, A., and McMahon, A. P. (2016) Differential regulation of mouse and human nephron progenitors by the Six family of transcriptional regulators. Development 143, 595-608
33. Walkin, L., Herrick, S.E., Summers, A., Brenchley, P. E., Hoff, C. M., Korstanje, R., and Margetts, P. J. (2013) The role of mouse strain differences in the susceptibility to fibrosis: a systematic review. Fibrogenesis Tissue Repair 6, 18
34. Wang, W., Wang, Y., Long, J., Wang, J., Haudek, S. B., Overbeek, P., Chang, B. H., Schumacker, P. T., and Danesh, F. R. (2012) Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab. 15, 186-200
35. Coimbra, T. M., Janssen, U., Gröne, H. J., Ostendorf, T., Kunter, U., Schmidt, H., Brabant, G., and Floege, J. (2000) Early events leading to renal injury in obese Zucker (fatty) rats with type II diabetes. Kidney Int. 57, 167-182
36. Ostojić, J., Panozzo, C., Lasserre, J. P., Nouet, C., Courtin, F., Blancard, C., di Rago, J. P., and Dujardin, G. (2013) The energetic state of mitochondria modulates complex III biogenesis through the ATPdependent activity of Bcs1. Cell Metab. 18, 567-577
37. Sieber, J., andJehle, A.W. (2014) Free fatty acids andtheirmetabolism affect function and survival of podocytes. Front. Endocrinol. (Lausanne) 5, 186
38. Hock, M. B., and Kralli, A. (2009) Transcriptional control of mitochondrial biogenesis and function. Annu. Rev. Physiol. 71, 177-203
39. Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D. M., Bŕethes, D., di Rago, J. P., and Velours, J. (2002) The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221-230
40. Carraro, M., Giorgio, V., Sǐleikyte , J., Sartori, G., Forte, M., Lippe, G., Zoratti, M., Szabó, I., and Bernardi, P. (2014) Channel formation by yeast F-ATP synthase and the role of dimerization in the mitochondrial permeability transition. J. Biol. Chem. 289, 15980-15985
41. Jose, C., Bellance, N., and Rossignol, R. (2011) Choosing between glycolysis andoxidativephosphorylation: a tumor's dilemma? Biochim. Biophys. Acta 1807, 552-561
42. Marfella, R., Quagliaro, L., Nappo, F., Ceriello, A., and Giugliano, D. (2001) Acute hyperglycemia induces an oxidative stress in healthy subjects. J. Clin. Invest. 108, 635-636
43. Nishikawa, T., and Araki, E. (2007) Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid. Redox Signal. 9, 343-353
44. Lambers Heerspink, H. J., and de Zeeuw, D. (2013) Novel drugs and interventionstrategies for the treatment of chronic kidney disease. Br. J. Clin. Pharmacol. 76, 536-550
45. McGee, S.L., andHargreaves, M. (2006)Exercise and skeletalmuscle glucose transporter 4 expression: molecular mechanisms. Clin. Exp. Pharmacol. Physiol. 33, 395-399
46. Lizcano, J. M., Göransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Mäkelä, T. P., Hardie, D. G., and Alessi, D.R. (2004) LKB1 is amaster kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843
47. Zong, H., Ren, J.M., Young, L.H., Pypaert, M., Mu, J., Birnbaum, M. J., and Shulman, G. I. (2002) AMP kinase is required formitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc.Natl. Acad. Sci. USA 99, 15983-15987
48. Panda, A. C., Abdelmohsen, K., Martindale, J. L., Di Germanio, C., Yang, X., Grammatikakis, I., Noh, J. H., Zhang, Y., Lehrmann, E., Dudekula, D. B., De, S., Becker, K. G., White, E. J., Wilson, G. M., de Cabo, R., and Gorospe, M. (2016) Novel RNA-binding activity of MYF5 enhances Ccnd1/Cyclin D1 mRNA translation during myogenesis. Nucleic Acids Res. 44, 2393-2408
49. Kim, J. W., Tchernyshyov, I., Semenza, G. L., and Dang, C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185
50. Xu, J., Han, J., Epstein, P.N., and Liu, Y.Q. (2006)Regulation of PDK mRNA by high fatty acid and glucose in pancreatic islets. Biochem. Biophys. Res. Commun. 344, 827-833
51. Gödel, M., Hartleben, B., Herbach, N., Liu, S., Zschiedrich, S., Lu, S., Debreczeni-Mór, A., Lindenmeyer, M.T., Rastaldi, M. P., Hartleben, G., Wiech, T., Fornoni, A., Nelson, R. G., Kretzler, M., Wanke, R., Pavensẗadt, H., Kerjaschki, D., Cohen, C. D., Hall, M. N., Rüegg, M.A., Inoki, K., Walz, G., and Huber, T. B. (2011) Role of mTOR in podocyte function and diabetic nephropathy in humans and mice. J. Clin. Invest. 121, 2197-2209
52. Inoki, K., Mori, H., Wang, J., Suzuki, T., Hong, S., Yoshida, S., Blattner, S. M., Ikenoue, T., Rüegg, M. A., Hall, M. N., Kwiatkowski, D. J., Rastaldi, M. P., Huber, T. B., Kretzler, M., Holzman, L. B., Wiggins, R. C., and Guan, K. L. (2011) mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J. Clin. Invest. 121, 2181-2196
53. Yan, K., Ito, N., Nakajo, A., Kurayama, R., Fukuhara, D., Nishibori, Y., Kudo, A., Akimoto, Y., and Takenaka, H. (2012) The struggle for energy in podocytes leads to nephrotic syndrome. Cell Cycle 11, 1504-1511
54. Lee, M. J., Feliers, D., Sataranatarajan, K., Mariappan, M. M., Li, M., Barnes, J.L., Choudhury, G. G., andKasinath, B. S. (2010)Resveratrol ameliorates high glucose-induced protein synthesis in glomerular epithelial cells. Cell. Signal. 22, 65-70
55. Yuan, Y., Huang, S., Wang, W., Wang, Y., Zhang, P., Zhu, C., Ding, G., Liu, B., Yang, T., and Zhang, A. (2012) Activation of peroxisome proliferator-activated receptor-g coactivator 1a ameliorates mitochondrial dysfunction and protects podocytes from ldosteroneinduced injury. Kidney Int. 82, 771-789