Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Diabetic Nephropathy - a Review of Risk Factors, Progression, Mechanism, and Dietary Management

  • Natesan, Vijayakumar (Department of Biochemistry and Biotechnology, Faculty of Science, Annamalai University) ;
  • Kim, Sung-Jin (Department of Pharmacology and Toxicology, Metabolic Diseases Research Laboratory, School of Dentistry, Kyung Hee University)
  • Received : 2020.11.11
  • Accepted : 2021.03.26
  • Published : 2021.07.01
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Abstract

Type 2 diabetes mellitus (T2DM) leads to many health problems like diabetic nephropathy (DN). One of the key factors for chronic kidney disease and end-stage renal disease (ESRD) is T2DM. Extensive work is being done to delineate the pathogenesis of DN and to extend possible remedies. This review is intended to understand the nature of DN risk factors, progression, effects of glycemic levels, and stages of DN. We also explored the novel diagnostic and therapeutic approaches for DN such as gene therapy and stem cell treatments.

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References

  1. Ahmad, T., Ulhaq, I., Mawani, M. and Islam, N. (2017) Microalbuminuria in type-2 diabetes mellitus; the tip of iceberg of diabetic complications. Pak. J. Med. Sci. 33, 519-523.
  2. Ahola, K. A. J., Forsblom, C. and Groop, P. H. (2018) Adherence to special diets and its association with meeting the nutrient recommendations in individuals with type 1 diabetes. Acta Diabetol. 55, 843-851. https://doi.org/10.1007/s00592-018-1159-2
  3. Amalan, V. and Vijayakumar, N. (2015) Antihyperglycemic effect of p-coumaric acid on streptozotocin induced diabetic rats. Indian J. Appl. Res. 5, 2249-2255.
  4. Amalan, V., Vijayakumar, N. and Ramakrishnan, A. (2015) p-Coumaric acid regulates blood glucose and antioxidant levels in streptozotocin induced diabetic rats. J. Chem. Pharm. Res. 7, 831-839.
  5. Anders, H. J., Davis, J. M. and Thurau, K. (2016) Nephron protection in diabetic kidney disease. N. Engl. J. Med. 375, 2096-2098. https://doi.org/10.1056/NEJMcibr1608564
  6. Azizi, M., Menard, J., Bissery, A., Guyene, T. T. and Bura-Riviere, A. (2007) Hormonal and hemodynamic effects of aliskiren and valsartan and their combination in sodium-replete normotensive individuals. Clin. J. Am. Soc. 2, 947-955.
  7. Berhane, A. M., Weil, E. J., Knowler, W. C., Nelson, R. G. and Hanson, R. L. (2011) Albuminuria and estimated glomerular filtration rate as predictors of diabetic end-stage renal disease and death. Clin. J. Am. Soc. Nephrol. 6, 2444-2451. https://doi.org/10.2215/CJN.00580111
  8. Bohman, S. O., Tyden, G., Wilczek, H., Lundgren, G., Jaremko, G., Gunnarsson, R., Ostman, J. and Groth, C. G. (1985) Prevention of kidney graft diabetic nephropathy by pancreas transplantation in man. Diabetes 34, 306-308. https://doi.org/10.2337/diabetes.34.3.306
  9. Bonora, E., Evangelisti, C., Bonichon, F., Tallini, G. and Romeo, G. (2006) Novel germline variants identified in the inner mitochondrial membrane transporter TIMM44 and their role in predisposition to oncocytic thyroid carcinomas. Br. J. Cancer 95, 1529-1536. https://doi.org/10.1038/sj.bjc.6603455
  10. Bornhorst, C., Russo, P., Veidebaum, T., Tornaritis, M., Molnar, D., Lissner, L., Marild, S., De Henauw, S., Moreno, L. A., Floegel, A., Ahrens, W. and Wolters, M. (2020) The role of lifestyle and non-modifiable risk factors in the development of metabolic disturbances from childhood to adolescence. Int. J. Obes. (Lond.) 44, 2236-2245. https://doi.org/10.1038/s41366-020-00671-8
  11. Caramori, M. L., Fioretto, P. and Mauer, M. (2000) The need for early predictors of diabetic nephropathy risk: is albumin excretion rate sufficient? Diabetes 49, 1399-1408. https://doi.org/10.2337/diabetes.49.9.1399
  12. Chatzikyrkou, C., Menne, J., Izzo, J., Viberti, G., Rabelink, T., Ruilope, L. M., Rump, C., Mertens, P. R. and Haller, H. (2017) Predictors for the development of microalbuminuria and interaction with renal function. J. Hypertens 35, 2501-2509. https://doi.org/10.1097/HJH.0000000000001491
  13. Chou, K. M., Lee, C. C., Chen, C. H. and Sun, C. Y. (2013) Clinical value of NGAL, L-FABP and albuminuria in predicting GFR decline in type 2 diabetes mellitus patients. PLoS ONE 8, e54863. https://doi.org/10.1371/journal.pone.0054863
  14. Conway, B. R., Manoharan, D., Manoharan, D, Jenks, S., Dear, J. W., McLachlan, S., Strachan, M. W. and Price, J. F. (2012) Measuring urinary tubular biomarkers in type 2 diabetes does not add prognostic value beyond established risk factors. Kidney Int. 82, 812-818. https://doi.org/10.1038/ki.2012.218
  15. Dande, R. R., Peev, V., Altintas, M. M. and Reiser, J. (2017) Soluble urokinase receptor and the kidney response in diabetes mellitus. J. Diabetes Res. 2017, 3232848.
  16. De Sanctis, V., Incorvaia, C., Soliman, A. T., Candini, G., Pepe, A., Kattamis, C., Soliman, N. A., Elsedfy, H. and Kholy, M. E. (2015) Does insulin like growth factor-1 (IGF-1) deficiency have a "protective" role in the development of diabetic retinopathy in thalassamia major patients? Mediterr. J. Hematol. Infect. Dis. 7, e2015038. https://doi.org/10.4084/mjhid.2015.038
  17. Dellamea, B. S., Pinto, L. C., Leitao, C. B., Santos, K. G. and Canani, L. H. (2014) Endothelial nitric oxide synthase gene polymorphisms and risk of diabetic nephropathy: a systematic review and meta-analysis. BMC Med. Genet. 15, 9.
  18. Eberhard, J., Drosos, Z., Tiemann, M., Jepsen, S. and Schroder, J. M. (2006) Immunolocalization of lactoferrin in healthy and inflamed gingival tissues. J. Periodontol. 77, 472-478. https://doi.org/10.1902/jop.2006.050186
  19. Fioretto, P., Steffes, M. W., Sutherland, D. E., Goetz, F. C. and Mauer, M. (1998) Reversal of lesions of diabetic nephropathy after pancreas transplantation. N. Engl. J. Med. 339, 69-75. https://doi.org/10.1056/NEJM199807093390202
  20. Fioretto, P., Sutherland, D. E., Najafian, B. and Mauer, M. (2006) Remodeling of renal interstitial and tubular lesions in pancreas transplant recipients. Kidney Int. 69, 907-912. https://doi.org/10.1038/sj.ki.5000153
  21. Fu, H., Liu, S., Bastacky, S. I., Wang, X., Tian, X. J. and Zhou, D. (2019) Diabetic kidney diseases revisited: a new perspective for a new era. Mol. Metab. 30, 250-263. https://doi.org/10.1016/j.molmet.2019.10.005
  22. Gall, M. A., Hougaard, P., Borch-Johnsen, K. and Parving, H. H. (1997) Risk factors for development of incipient and overt diabetic nephropathy in patients with non-insulin dependent diabetes mellitus: prospective, observational study. BMJ 314, 783-788. https://doi.org/10.1136/bmj.314.7083.783
  23. Gentile, G., Mastroluca, D., Ruggenenti, P. and Remuzzi, G. (2014) Novel effective drugs for diabetic kidney disease? or not? Expert Opin. Emerg. Drugs 19, 571-601. https://doi.org/10.1517/14728214.2014.979151
  24. Gheith, O., Farouk, N., Nampoory, N., Halim, M. A. and Al-Otaibi, T. (2016) Diabetic kidney disease: world wide difference of prevalence and risk factors. J. Nephropharmacol. 5, 49-56.
  25. Gonzalez, D. E., Foresto, R. D. and Ribeiro, A. B. (2020) SGLT-2 inhibitors in diabetes: a focus on renoprotection. Rev. Assoc. Med. Bras. 66, s17-s24. https://doi.org/10.1590/1806-9282.66.s2.17
  26. Hill, N. R., Fatoba, S. T., Oke, J. L., Hirst, J. A., O'Callaghan, C. A., Lasserson, D. S. and Hobbs, F. D. R. (2016) Global prevalence of chronic kidney disease - a systematic review and meta-analysis. PLoS ONE 11, e0158765. https://doi.org/10.1371/journal.pone.0158765
  27. Kanauchi, N., Ookawara, S., Ito, K., Mogi, S., Yoshida, I., Kakei, M., Ishikawa, S. E., Morishita, Y. and Tabei, K. (2015) Factors affecting the progression of renal dysfunction and the importance of salt restriction in patients with type 2 diabetic kidney disease. Clin. Exp. Nephrol. 19, 1120-1126. https://doi.org/10.1007/s10157-015-1118-y
  28. Kim, H. Y. (2014) Nutritional intervention for a patient with diabetic nephropathy. Clin. Nutr. Res. 3, 64-68. https://doi.org/10.7762/cnr.2014.3.1.64
  29. Kim, S. S., Song, S. H., Kim, I. J., Jeon, Y. K., Kim, B. H., Kwak, I. S., Lee, E. K. and Kim, Y. K. (2013) Urinary cystatin C and tubular proteinuria predict progression of diabetic nephropathy. Diabetes Care 36, 656-661. https://doi.org/10.2337/dc12-0849
  30. Kitada, M., Ogura, Y., Monno, I. and Koya, D. (2018) A low-protein diet for diabetic kidney disease: its effect and molecular mechanism, an approach from animal studies. Nutrients 10, 544. https://doi.org/10.3390/nu10050544
  31. Kopel, J., Pena-Hernandez, C. and Nugent, K. (2019) Evolving spectrum of diabetic nephropathy. World J. Diabetes 10, 269-279. https://doi.org/10.4239/wjd.v10.i5.269
  32. Krock, B. L., Skuli, N. and Simon, M. C. (2011) Hypoxia-induced angiogenesis: good and evil. Genes Cancer 2, 1117-1133. https://doi.org/10.1177/1947601911423654
  33. Lacquaniti, A., Donato, V., Pintaudi, B., Di Vieste, G., Chirico, V., Buemi, A., Di Benedetto, A., Arena, A. and Buemi, M. (2013) "Normoalbuminuric" diabetic nephropathy: tubular damage and NGAL. Acta Diabetol. 50, 935-942. https://doi.org/10.1007/s00592-013-0485-7
  34. Lerner, S. M. (2008) Kidney and pancreas transplantation in type 1 diabetes mellitus. Mt. Sinai J. Med. 75, 372-384. https://doi.org/10.1002/msj.20056
  35. Li, J. Y., Chen, X. X., Lu, X. H., Zhang, C. B., Shi, Q. P. and Feng, L. (2018) Elevated RBP4 plasma levels were associated with diabetic retinopathy in type 2 diabetes. Biosci. Rep. 38, BSR20181100. https://doi.org/10.1042/BSR20181100
  36. Liu, A. G., Ford, N. A., Hu, F. B., Zelman, K. M., Mozaffarian, D. and Kris-Etherton, P. M. (2017) A healthy approach to dietary fats: understanding the science and taking action to reduce consumer confusion. Nutr. J. 16, 53. https://doi.org/10.1186/s12937-017-0271-4
  37. Liu, D., Cheng, F., Pan, S. and Liu, Z. (2020) Stem cells: a potential treatment option for kidney diseases. Stem Cell Res. Ther. 11, 249. https://doi.org/10.1186/s13287-020-01751-2
  38. Lu, B., Wen, J., Song, X. Y., Dong, X. H., Yang, Y. H., Zhang, Z. Y., Zhao, N. Q., Ye, H. Y., Mou, B., Chen, F. L., Liu, Y., Shen, Y., Wang, X. C., Zhou, L. N., Li, Y. M., Zhu, X. X. and Hu, R. M. (2017) High prevalence of albuminuria in population-based patients diagnosed with type 2 diabetes in the Shanghai downtown. Diabetes Res. Clin. Pract. 75, 184-192. https://doi.org/10.1016/j.diabres.2006.06.024
  39. Mohammad, G. and Siddiquei, M. M. (2012) Role of matrix metalloproteinase-2 and -9 in the development of diabetic retinopathy. J. Ocul. Biol. Dis. Infor. 5, 1-8. https://doi.org/10.1007/s12177-012-9091-0
  40. Motawi, T. K., Shehata, N. I., ElNokeety, M. M. and El-Emady, Y. F. (2018) Potential serum biomarkers for early detection of diabetic nephropathy. Diabetes Res. Clin. Pract. 136, 150-158. https://doi.org/10.1016/j.diabres.2017.12.007
  41. Mussbacher, M., Salzmann, M., Brostjan, C., Hoesel, B., Schoergenhofer, C., Datler, H., Hohensinner, P., Basilio, J., Petzelbauer, P., Assinger, A. and Schmid, J. A. (2019) Cell type-specific roles of NF-κB linking inflammation and thrombosis. Front. Immunol. 10, 85. https://doi.org/10.3389/fimmu.2019.00085
  42. Narres, M., Claessen, H., Droste, S., Kvitkina, T., Koch, M., Kuss, O. and Icks, A. (2016) The incidence of end-stage renal disease in the diabetic (compared to the non-diabetic) population: a systematic review. PLoS ONE 11, e0147329. https://doi.org/10.1371/journal.pone.0147329
  43. Navarro, J. F., Milena, F. J., Mora, C., Leon, C., Claverie, F., Flores, C. and Garcia, J. (2005) Tumor necrosis factor-alpha gene expression in diabetic nephropathy: relationship with urinary albumin excretion and effect of angiotensin-converting enzyme inhibition. Kidney Int. Suppl. (99), S98-S102.
  44. Neal, B., Perkovic, V., Mahaffey, K. W., de Zeeuw, D., Fulcher, G., Erondu, N., Shaw, W., Law, G., Desai, M. and Matthews, D. R.; CANVAS Program Collaborative Group (2017) Canagliflozin and cardiovascular and renal events in type 2 diabetes. N. Engl. J. Med. 377, 644-657. https://doi.org/10.1056/NEJMoa1611925
  45. Nielsen, H. B., Almeida, M., Juncker, A. S., Rasmussen, S., Li, J., Sunagawa, S., Plichta, D. R., Gautier, L., Pedersen, A. G., Le Chatelier, E., Pelletier, E., Bonde, I., Nielsen, T., Manichanh, C., Arumugam, M., Batto, J. M., Quintanilha Dos Santos, M. B., Blom, N., Borruel, N., Burgdorf, K. S., Boumezbeur, F., Casellas, F., Dore, J., Dworzynski, P., Guarner, F., Hansen, T., Hildebrand, F., Kaas, R. S., Kennedy, S., Kristiansen, K., Kultima, J. R., Leonard, P., Levenez, F., Lund, O., Moumen, B., Le Paslier, D., Pons, N., Pedersen, O., Prifti, E., Qin, J., Raes, J., Sorensen, S., Tap, J., Tims, S., Ussery, D. W., Yamada, T.; MetaHIT Consortium, Renault, P., Sicheritz-Ponten, T., Bork, P., Wang, J., Brunak, S., Ehrlich, S. D. (2014) Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822-828. https://doi.org/10.1038/nbt.2939
  46. Nielsen, S. E., Andersen, S., Zdunek, D., Hess, G., Parving, H. H. and Rossing, P. (2011) Tubular markers do not predict the decline in glomerular filtration rate in type 1 diabetic patients with overt nephropathy. Kidney Int. 79, 1113-1118. https://doi.org/10.1038/ki.2010.554
  47. Niewczas, M. A., Gohda, T., Skupien, J., Smiles, A. M., Walker, W. H., Rosetti, F., Cullere, X., Eckfeldt, J. H., Doria, A., Mayadas, T. N., Warram, J. H. and Krolewski, A. S. (2012) Circulating TNF receptors 1 and 2 predict ESRD in type 2 diabetes. J. Am. Soc. Nephrol. 23, 507-515. https://doi.org/10.1681/ASN.2011060627
  48. Oates, P. J. (2010) Aldose reductase inhibitors and diabetic kidney disease. Curr. Opin. Investig. Drugs 11, 402-417.
  49. Oh, S. W., Kim, S., Na, K. Y., Chae, D. W., Kim, S., Jin, D. C. and Chin, H. J. (2012) Clinical implications of pathologic diagnosis and classification for diabetic nephropathy. Diabetes Res. Clin. Pract. 97, 418-424. https://doi.org/10.1016/j.diabres.2012.03.016
  50. Oltean, S., Coward, R., Collino, M. and Baelde, H. (2017) Diabetic nephropathy: novel molecular mechanisms and therapeutic avenues. Biomed. Res. Int. 2017, 3146524.
  51. Otoda, T., Kanasaki, K. and Koya, D. (2014) Low-protein diet for diabetic nephropathy. Curr. Diab. Rep. 14, 523. https://doi.org/10.1007/s11892-014-0523-z
  52. Panduru, N. M., Forsblom, C., Saraheimo, M., Thorn, L., Bierhaus, A., Humpert, P. M. and Groop, P. H.; FinnDiane Study Group (2013) Urinary liver-type fatty acid-binding protein and progression of diabetic nephropathy in type 1 diabetes. Diabetes Care 36, 2077-2083. https://doi.org/10.2337/dc12-1868
  53. Papadopoulou-Marketou, N., Kanaka-Gantenbein, C., Marketos, N., Chrousos, G. P. and Papassotiriou, I. (2017) Biomarkers of diabetic nephropathy: a 2017 update. Crit. Rev. Clin. Lab. Sci. 54, 326-342. https://doi.org/10.1080/10408363.2017.1377682
  54. Perry, R. J. and Shulman, G. I. (2020) Sodium-glucose cotransporter-2 inhibitors: understanding the mechanisms for therapeutic promise and persisting risks. J. Biol. Chem. 295, 14379-14390. https://doi.org/10.1074/jbc.rev120.008387
  55. Petrie Aronin, C. E. and Tuan, R. S. (2010) Therapeutic potential of the immunomodulatory activities of adult mesenchymal stem cells. Birth Defects Res. C Embryo Today 90, 67-74. https://doi.org/10.1002/bdrc.20174
  56. Pettitt, D. J., Saad, M. F., Bennett, P. H., Nelson, R. G. and Knowler, W. C. (1990) Familial predisposition to renal disease in two generations of Pima Indians with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 33, 438-443. https://doi.org/10.1007/BF00404096
  57. Pugliese, G., Penno, G., Natali, A., Barutta, F., Di Paolo, S., Reboldi, G., Gesualdo, L. and De Nicola, L.; Italian Diabetes Society and the Italian Society of Nephrology (2020) Diabetic kidney disease: new clinical and therapeutic issues. Joint position statement of the Italian Diabetes Society and the Italian Society of Nephrology on "The natural history of diabetic kidney disease and treatment of hyperglycemia in patients with type 2 diabetes and impaired renal function". J. Nephrol. 33, 9-35. https://doi.org/10.1007/s40620-019-00650-x
  58. Kowluru, R. A. (2010) Role of Matrix metalloproteinase-9 in the development of diabetic retinopathy and its regulation by H-ras. Invest. Ophthalmol. Vis. Sci. 51, 4320-4326. https://doi.org/10.1167/iovs.09-4851
  59. Retnakaran, R., Cull, C. A., Thorne, K. I., Adler, A. I. and Holman, R. R.; UKPDS Study Group (2006) Risk factors for renal dysfunction in type 2 diabetes: U.K. prospective diabetes study 74. Diabetes 55, 1832-1839. https://doi.org/10.2337/db05-1620
  60. Rojas, M. A., Zhang, W., Xu, Z., Nguyen, D. T., Caldwell, R. W. and Caldwell, R. B. (2011) Interleukin 6 has a critical role in diabetesinduced retinal vascular inflammation and permeability. Invest. Ophthalmol. Vis. Sci. 52, 1003. https://doi.org/10.1167/iovs.10-5375
  61. Rota, C., Morigi, M. and Imberti, B. (2019) Stem cell therapies in kidney diseases: progress and challenges. Int. J. Mol. Sci. 20, 2790. https://doi.org/10.3390/ijms20112790
  62. Sabbisetti, V. S., Waikar, S. S., Antoine, D. J., Smiles, A., Wang, C., Ravisankar, A., Ito, K., Sharma, S., Ramadesikan, S., Lee, M., Briskin, R., De Jager, P. L., Ngo, T. T., Radlinski, M., Dear, J. W., Park, K. B., Betensky, R., Krolewski, A. S. and Bonventre, J. V. (2014) Blood kidney injury molecule-1 is a biomarker of acute and chronic kidney injury and predicts progression to ESRD in type I diabetes. J. Am. Soc. Nephrol. 25, 2177-2186. https://doi.org/10.1681/ASN.2013070758
  63. Saran, R., Robinson, B., Abbott, K. C., Agodoa, L. Y., Albertus, P., Ayanian, J., Balkrishnan, R., Bragg-Gresham, J., Cao, J., Chen, J. L., Cope, E., Dharmarajan, S., Dietrich, X., Eckard, A., Eggers, P. W., Gaber, C., Gillen, D., Gipson, D., Gu, H., Hailpern, S. M., Hall, Y. N., Han, Y., He, K., Hebert, H., Helmuth, M., Herman, W., Heung, M., Hutton, D., Jacobsen, S. J., Ji, N., Jin, Y., Kalantar-Zadeh, K., Kapke, A., Katz, R., Kovesdy, C. P., Kurtz, V., Lavalee, D., Li, Y., Lu, Y., McCullough, K., Molnar, M. Z., Montez-Rath, M., Morgenstern, H., Mu, Q., Mukhopadhyay, P., Nallamothu, B., Nguyen, D. V., Norris, K. C., O'Hare, A. M., Obi, Y., Pearson, J., Pisoni, R., Plattner, B., Port, F. K., Potukuchi, P., Rao, P., Ratkowiak, K., Ravel, V., Ray, D., Rhee, C. M., Schaubel, D. E., Selewski, D. T., Shaw, S., Shi, J., Shieu, M., Sim, J. J., Song, P., Soohoo, M., Steffick, D., Streja, E., Tamura, M. K., Tentori, F., Tilea, A., Tong, L., Turf, M., Wang, D., Wang, M., Woodside, K., Wyncott, A., Xin, X., Zang, W., Zepel, L., Zhang, S., Zho, H., Hirth, R. A. and Shahinian, V. (2017) US Renal Data System 2016 Annual Data Report: epidemiology of kidney disease in the United States. Am. J. Kidney Dis. 69, A7-A8. https://doi.org/10.1053/S0272-6386(17)30043-4
  64. Satko, S. G., Langefeld, C. D., Daeihagh, P., Bowden, D. W., Rich, S. S. and Freedman, B. I. (2002) Nephropathy in siblings of African Americans with overt type 2 diabetic nephropathy. Am. J. Kidney Dis. 40, 489-494. https://doi.org/10.1053/ajkd.2002.34888
  65. Schrijvers, B. F., De Vriese, A. S. and Flyvbjerg, A. (2004) From hyperglycemia to diabetic kidney disease: the role of metabolic, hemodynamic, intracellular factors and growth factors/cytokines. Endocr. Rev. 25, 971-1010. https://doi.org/10.1210/er.2003-0018
  66. Scott, L. J., Warram, J. H., Hanna, L. S., Laffel, L. M., Ryan, L. and Krolewski, A. S. (2001) A nonlinear effect of hyperglycemia and current cigarette smoking are major determinants of the onset of microalbuminuria in type 1 diabetes. Diabetes 50, 2842-2849. https://doi.org/10.2337/diabetes.50.12.2842
  67. Shahbazian, H. and Rezaii, I. (2013) Diabetic kidney disease; review of the current knowledge. J. Renal Inj. Prev. 2, 73-80.
  68. Skupien, J., Warram, J. H., Smiles, A., Galecki, A., Stanton, R. C. and Krolewski, A. S. (2014) Improved glycemic control and risk of ESRD in patients with type 1 diabetes and proteinuria. J. Am. Soc. Nephrol. 25, 2916-2925. https://doi.org/10.1681/asn.2013091002
  69. Smith, A. and Harris, C. (2018) Type 1 diabetes: management strategies. Am. Fam. Physician 98, 154-162.
  70. Sulaiman, M. K. (2019) Diabetic nephropathy: recent advances in pathophysiology and challenges in dietary management. Diabetol. Metab. Syndr. 11, 7. https://doi.org/10.1186/s13098-019-0403-4
  71. Taylor, R. W. and Turnbull, D. M. (2005) Mitochondrial DNA mutations in human disease. Nat. Rev. Genet. 6, 389-402. https://doi.org/10.1038/nrg1606
  72. Tervaert, T. W., Mooyaart, A. L., Amann, K., Cohen, A. H., Cook, H. T., Drachenberg, C. B., Ferrario, F., Fogo, A. B., Haas, M., de Heer, E., Joh, K., Noel, L. H., Radhakrishnan, J., Seshan, S. V., Bajema, I. M. and Bruijn, J. A.; Renal Pathology Society (2010) Pathologic classification of diabetic nephropathy. J. Am. Soc. Nephrol. 21, 556-563. https://doi.org/10.1681/ASN.2010010010
  73. Tonneijck, L., Muskiet, M. H. A., Smits, M. M., van Bommel, E. J., Heerspink, H. J. L., van Raalte, D. H. and Joles, J. A. (2017) Glomerular hyperfiltration in diabetes: mechanisms, clinical significance, and treatment. J. Am. Soc. Nephrol. 28, 1023-1039. https://doi.org/10.1681/ASN.2016060666
  74. Trimeche, A., Selmi, Y., Ben Slama. F., Ben Amara, H., Hazar, I., Ben Mami, F. and Achour, A. (2013) Effect of protein restriction on renal function and nutritional status of type 1 diabetes at the stage of renal impairment. Tunis. Med. 91, 117-122.
  75. Vallon, V. (2015) The mechanisms and therapeutic potential of SGLT2 inhibitors in diabetes mellitus. Annu. Rev. Med. 66, 255-270. https://doi.org/10.1146/annurev-med-051013-110046
  76. Wada, J., Makino, H. and Kanwar, Y. S. (2002) Gene expression and identification of gene therapy targets in diabetic nephropathy. Kidney Int. 61, S73-S78.
  77. Wallner, E. I., Wada, J., Lin, S., Pan, X., Reddy, J. K., Chugh, S. S. and Kanwar, Y. S. (2002) Renal gene expression in embryonic and newborn diabetic mice. Exp. Nephrol. 10, 130-138. https://doi.org/10.1159/000049908
  78. Wanner, C., Inzucchi, S. E., Lachin, J. M., Fitchett, D., von Eynatten, M., Mattheus, M., Johansen, O. E., Woerle, H. J., Broedl, U. C. and Zinman, B.; EMPA-REG OUTCOME Investigators (2016) Empagliflozin and progression of kidney disease in type 2 diabetes. N. Engl. J. Med. 375, 323-334. https://doi.org/10.1056/NEJMoa1515920
  79. Werner, N., Nickenig, G. and Sinning, J. M. (2018) Complex PCI procedures: challenges for the interventional cardiologist. Clin. Res. Cardiol. 107, 64-73. https://doi.org/10.1007/s00392-018-1316-1
  80. Young, B. A., Maynard, C. and Boyko, E. J. (2003) Racial differences in diabetic nephropathy, cardiovascular disease, and mortality in a national population of veterans. Diabetes Care 26, 2392-2399. https://doi.org/10.2337/diacare.26.8.2392
  81. Zakrzewski, W., Dobrzynski, M., Szymonowicz, M. and Rybak, Z. (2019) Stem cells: past, present, and future. Stem Cell Res. Ther. 10, 68. https://doi.org/10.1186/s13287-019-1165-5
  82. Zeni, L., Norden, A. G. W., Cancarini, G. and Unwin, R. J. (2017) A more tubulocentric view of diabetic kidney disease. J. Nephrol. 30, 701-717. https://doi.org/10.1007/s40620-017-0423-9
  83. Zha, Y. and Qian, Q. (2017) Protein nutrition and malnutrition in CKD and ESRD. Nutrients 9, 208. https://doi.org/10.3390/nu9030208

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