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The Interconnection Between Immuno-Metabolism, Diabetes, and CKD

  • Microvascular Complications—Nephropathy (M Afkarian and B Roshanravan, Section Editors)
  • Published:
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Abstract

Purpose of Review

Metabolic reprogramming is increasingly recognized as an essential trait of functional activation of immune cells. Here, we describe the link between immuno-metabolism, diabetes, and diabetic nephropathy.

Recent Findings

Crosstalk between cellular metabolic functions and immune activation occurs when plasma levels of glucose, triglycerides, and free fatty acids increase, thus promoting systemic low-grade inflammation that further boosts the development of metabolic complications. In the long run, this settles an “apparent paradox,” where, despite excessive inflammation, the immune system is suppressed, further promoting progression to end-stage renal disease (ESRD) and predisposing to premature deaths from infections and cardiovascular diseases. Reviewing the effects of diabetes treatments on immuno-inflammatory responses suggests that the benefit of these drugs might extend beyond the simple control of glucose homeostasis.

Summary

Hyperglycemia and dyslipidemia correlate with enhancement of the immuno-inflammatory response that can promote and worsen metabolic diseases and support the progression toward ESRD. The identification of cellular checkpoints that modulate the immuno-metabolic machinery of immune cells opens new venues for metabolic drugs.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. •• Norata GD, Caligiuri G, Chavakis T, Matarese G, Netea MG, Nicoletti A, et al. The cellular and molecular basis of translational immuno-metabolism. Immunity. 2015;43(3):421–34. https://doi.org/10.1016/j.immuni.2015.08.023. This review discusses from a translational perspective the connection between cellular metabolism and immune cell activations.

    Article  CAS  PubMed  Google Scholar 

  2. Tomas E, Lin YS, Dagher Z, Saha A, Luo Z, Ido Y, et al. Hyperglycemia and insulin resistance: possible mechanisms. Ann N Y Acad Sci. 2002;967:43–51.

    Article  CAS  PubMed  Google Scholar 

  3. Zmora N, Bashiardes S, Levy M, Elinav E. The role of the immune system in metabolic health and disease. Cell Metab. 2017;25(3):506–21. https://doi.org/10.1016/j.cmet.2017.02.006.

    Article  CAS  PubMed  Google Scholar 

  4. Ellulu MS, Patimah I, Khaza'ai H, Rahmat A, Abed Y. Obesity and inflammation: the linking mechanism and the complications. Arch Med Sci. 2017;13(4):851–63. https://doi.org/10.5114/aoms.2016.58928.

    Article  CAS  PubMed  Google Scholar 

  5. Artunc F, Schleicher E, Weigert C, Fritsche A, Stefan N, Haring HU. The impact of insulin resistance on the kidney and vasculature. Nat Rev Nephrol. 2016;12(12):721–37. https://doi.org/10.1038/nrneph.2016.145.

    Article  CAS  PubMed  Google Scholar 

  6. Lee JY, Plakidas A, Lee WH, Heikkinen A, Chanmugam P, Bray G, et al. Differential modulation of toll-like receptors by fatty acids: preferential inhibition by n-3 polyunsaturated fatty acids. J Lipid Res. 2003;44(3):479–86. https://doi.org/10.1194/jlr.M200361-JLR200.

    Article  PubMed  Google Scholar 

  7. Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME. Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity. 2008;16(6):1248–55. https://doi.org/10.1038/oby.2008.210.

    Article  CAS  PubMed  Google Scholar 

  8. Oishi Y, Spann NJ, Link VM, Muse ED, Strid T, Edillor C, et al. SREBP1 contributes to resolution of pro-inflammatory TLR4 signaling by reprogramming fatty acid metabolism. Cell Metab. 2017;25(2):412–27. https://doi.org/10.1016/j.cmet.2016.11.009.

    Article  CAS  PubMed  Google Scholar 

  9. Souza CO, Teixeira AA, Biondo LA, Silveira LS, Calder PC, Rosa Neto JC. Palmitoleic acid reduces the inflammation in LPS-stimulated macrophages by inhibition of NFkappaB, independently of PPARs. Clin Exp Pharmacol Physiol. 2017;44(5):566–75. https://doi.org/10.1111/1440-1681.12736.

    Article  CAS  PubMed  Google Scholar 

  10. Carrillo C, Cavia Mdel M, Alonso-Torre S. Role of oleic acid in immune system; mechanism of action; a review. Nutr Hosp. 2012;27(4):978–90. https://doi.org/10.3305/nh.2012.27.4.5783.

    Article  CAS  PubMed  Google Scholar 

  11. Talbot NA, Wheeler-Jones CP, Cleasby ME. Palmitoleic acid prevents palmitic acid-induced macrophage activation and consequent p38 MAPK-mediated skeletal muscle insulin resistance. Mol Cell Endocrinol. 2014;393(1–2):129–42. https://doi.org/10.1016/j.mce.2014.06.010.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Tardif N, Salles J, Landrier JF, Mothe-Satney I, Guillet C, Boue-Vaysse C, et al. Oleate-enriched diet improves insulin sensitivity and restores muscle protein synthesis in old rats. Clin Nutr. 2011;30(6):799–806. https://doi.org/10.1016/j.clnu.2011.05.009.

    Article  CAS  PubMed  Google Scholar 

  13. Bernstein AM, Roizen MF, Martinez L. Purified palmitoleic acid for the reduction of high-sensitivity C-reactive protein and serum lipids: a double-blinded, randomized, placebo controlled study. J Clin Lipidol. 2014;8(6):612–7. https://doi.org/10.1016/j.jacl.2014.08.001.

    Article  PubMed  Google Scholar 

  14. • Singer K, DelProposto J, Morris DL, Zamarron B, Mergian T, Maley N, et al. Diet-induced obesity promotes myelopoiesis in hematopoietic stem cells. Mol Metab. 2014;3(6):664–75. https://doi.org/10.1016/j.molmet.2014.06.005. This paper highlights how obesity triggers activation and proliferation of progenitors cells contributing to adipose tissue inflammation.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Nagareddy PR, Kraakman M, Masters SL, Stirzaker RA, Gorman DJ, Grant RW, et al. Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity. Cell Metab. 2014;19(5):821–35. https://doi.org/10.1016/j.cmet.2014.03.029.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Yvan-Charvet L, Pagler T, Gautier EL, Avagyan S, Siry RL, Han S, et al. ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science. 2010;328(5986):1689–93. https://doi.org/10.1126/science.1189731.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Yvan-Charvet L, Welch C, Pagler TA, Ranalletta M, Lamkanfi M, Han S, et al. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation. 2008;118(18):1837–47. https://doi.org/10.1161/CIRCULATIONAHA.108.793869.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Westerterp M, Murphy AJ, Wang M, Pagler TA, Vengrenyuk Y, Kappus MS, et al. Deficiency of ATP-binding cassette transporters A1 and G1 in macrophages increases inflammation and accelerates atherosclerosis in mice. Circ Res. 2013;112(11):1456–65. https://doi.org/10.1161/CIRCRESAHA.113.301086.

    Article  CAS  PubMed  Google Scholar 

  19. Bonacina F, Coe D, Wang G, Longhi MP, Baragetti A, Moregola A, et al. Myeloid apolipoprotein E controls dendritic cell antigen presentation and T cell activation. Nat Commun. 2018;9(1):3083. https://doi.org/10.1038/s41467-018-05322-1.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Ito A, Hong C, Oka K, Salazar JV, Diehl C, Witztum JL, et al. Cholesterol accumulation in CD11c(+) immune cells is a causal and targetable factor in autoimmune disease. Immunity. 2016;45(6):1311–26. https://doi.org/10.1016/j.immuni.2016.11.008.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Kidani Y, Elsaesser H, Hock MB, Vergnes L, Williams KJ, Argus JP, et al. Sterol regulatory element-binding proteins are essential for the metabolic programming of effector T cells and adaptive immunity. Nat Immunol. 2013;14(5):489–99. https://doi.org/10.1038/ni.2570.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. • Mauro C, Smith J, Cucchi D, Coe D, Fu H, Bonacina F, et al. Obesity-induced metabolic stress leads to biased effector memory CD4(+) T cell differentiation via PI3K p110delta-Akt-mediated signals. Cell Metab. 2017;25(3):593–609. https://doi.org/10.1016/j.cmet.2017.01.008. This work identifies how fatty acids primed CD4+T cells activation resulting in increased circulating levels of T effector memory cells in obese individuals.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. O’Sullivan D, van der Windt GJ, Huang SC, Curtis JD, Chang CH, Buck MD, et al. Memory CD8(+) T cells use cell-intrinsic lipolysis to support the metabolic programming necessary for development. Immunity. 2014;41(1):75–88. https://doi.org/10.1016/j.immuni.2014.06.005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. • Sestan M, Marinovic S, Kavazovic I, Cekinovic D, Wueest S, Turk Wensveen T, et al. Virus-induced interferon-gamma causes insulin resistance in skeletal muscle and derails glycemic control in obesity. Immunity. 2018;49(1):164–77 e6. https://doi.org/10.1016/j.immuni.2018.05.005. This paper describes how immune response derails glucose homeostasis in pre-diabetic conditions.

    Article  CAS  PubMed  Google Scholar 

  25. Ghesquiere B, Wong BW, Kuchnio A, Carmeliet P. Metabolism of stromal and immune cells in health and disease. Nature. 2014;511(7508):167–76. https://doi.org/10.1038/nature13312.

    Article  CAS  PubMed  Google Scholar 

  26. Jha AK, Huang SC, Sergushichev A, Lampropoulou V, Ivanova Y, Loginicheva E, et al. Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization. Immunity. 2015;42(3):419–30. https://doi.org/10.1016/j.immuni.2015.02.005.

    Article  CAS  PubMed  Google Scholar 

  27. Soehnlein O, Swirski FK. Hypercholesterolemia links hematopoiesis with atherosclerosis. Trends Endocrinol Metab. 2013;24(3):129–36. https://doi.org/10.1016/j.tem.2012.10.008.

    Article  CAS  PubMed  Google Scholar 

  28. Nagareddy PR, Murphy AJ, Stirzaker RA, Hu Y, Yu S, Miller RG, et al. Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell Metab. 2013;17(5):695–708. https://doi.org/10.1016/j.cmet.2013.04.001.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Marino E, Richards JL, McLeod KH, Stanley D, Yap YA, Knight J, et al. Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes. Nat Immunol. 2017;18(5):552–62. https://doi.org/10.1038/ni.3713.

    Article  CAS  PubMed  Google Scholar 

  30. Zhang D, Chia C, Jiao X, Jin W, Kasagi S, Wu R, et al. D-mannose induces regulatory T cells and suppresses immunopathology. Nat Med. 2017;23(9):1036–45. https://doi.org/10.1038/nm.4375.

    Article  CAS  PubMed  Google Scholar 

  31. •• Zoccali C, Vanholder R, Massy ZA, Ortiz A, Sarafidis P, Dekker FW, et al. The systemic nature of CKD. Nat Rev Nephrol. 2017;13(6):344–58. https://doi.org/10.1038/nrneph.2017.52. A comprehensive review of the circuits linking renal disease to energy balance, immune response and neuroendocrine signalling.

    Article  PubMed  Google Scholar 

  32. Aroor AR, McKarns S, Demarco VG, Jia G, Sowers JR. Maladaptive immune and inflammatory pathways lead to cardiovascular insulin resistance. Metab Clin Exp. 2013;62(11):1543–52. https://doi.org/10.1016/j.metabol.2013.07.001.

    Article  CAS  PubMed  Google Scholar 

  33. Vaziri ND, Pahl MV, Crum A, Norris K. Effect of uremia on structure and function of immune system. J Ren Nutr. 2012;22(1):149–56. https://doi.org/10.1053/j.jrn.2011.10.020.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. • Kato S, Chmielewski M, Honda H, Pecoits-Filho R, Matsuo S, Yuzawa Y, et al. Aspects of immune dysfunction in end-stage renal disease. Clin J Am Soc Nephrol. 2008;3(5):1526–33. https://doi.org/10.2215/CJN.00950208. This review provides an integrate review about the alteration in immune response during kidney disease.

    Article  PubMed Central  PubMed  Google Scholar 

  35. • Obi Y, Qader H, Kovesdy CP, Kalantar-Zadeh K. Latest consensus and update on protein-energy wasting in chronic kidney disease. Curr Opin Clin Nutr Metab Care. 2015;18(3):254–62. https://doi.org/10.1097/MCO.0000000000000171. This is a consensus paper about the relevance of cachexia, malnutrition, and their pathological consequences in advanced renal disease.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Donath MY. When metabolism met immunology. Nat Immunol. 2013;14(5):421–2. https://doi.org/10.1038/ni.2591.

    Article  CAS  PubMed  Google Scholar 

  37. Shulman GI. Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease. N Engl J Med. 2014;371(23):2237–8. https://doi.org/10.1056/NEJMc1412427.

    Article  PubMed  Google Scholar 

  38. Malin SK, Finnegan S, Fealy CE, Filion J, Rocco MB, Kirwan JP. Beta-cell dysfunction is associated with metabolic syndrome severity in adults. Metab Syndr Relat Disord. 2014;12(2):79–85. https://doi.org/10.1089/met.2013.0083.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Cerf ME. Beta cell dysfunction and insulin resistance. Front Endocrinol. 2013;4:37. https://doi.org/10.3389/fendo.2013.00037.

    Article  Google Scholar 

  40. Guiteras R, Flaquer M, Cruzado JM. Macrophage in chronic kidney disease. Clin Kidney J. 2016;9(6):765–71. https://doi.org/10.1093/ckj/sfw096.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Wentworth JM, Fourlanos S, Harrison LC. Reappraising the stereotypes of diabetes in the modern diabetogenic environment. Nat Rev Endocrinol. 2009;5(9):483–9. https://doi.org/10.1038/nrendo.2009.149.

    Article  CAS  PubMed  Google Scholar 

  42. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107. https://doi.org/10.1038/nri2925.

    Article  CAS  PubMed  Google Scholar 

  43. Grossmann V, Schmitt VH, Zeller T, Panova-Noeva M, Schulz A, Laubert-Reh D, et al. Profile of the immune and inflammatory response in individuals with prediabetes and type 2 diabetes. Diabetes Care. 2015;38(7):1356–64. https://doi.org/10.2337/dc14-3008.

    Article  CAS  PubMed  Google Scholar 

  44. Moreno-Manzano V, Ishikawa Y, Lucio-Cazana J, Kitamura M. Selective involvement of superoxide anion, but not downstream compounds hydrogen peroxide and peroxynitrite, in tumor necrosis factor-alpha-induced apoptosis of rat mesangial cells. J Biol Chem. 2000;275(17):12684–91.

    Article  CAS  PubMed  Google Scholar 

  45. Gu HF, Ma J, Gu KT, Brismar K. Association of intercellular adhesion molecule 1 (ICAM1) with diabetes and diabetic nephropathy. Front Endocrinol. 2012;3:179. https://doi.org/10.3389/fendo.2012.00179.

    Article  Google Scholar 

  46. Di Marco E, Gray SP, Jandeleit-Dahm K. Diabetes alters activation and repression of pro- and anti-inflammatory signaling pathways in the vasculature. Front Endocrinol. 2013;4:68. https://doi.org/10.3389/fendo.2013.00068.

    Article  Google Scholar 

  47. Woltman AM, de Fijter JW, Zuidwijk K, Vlug AG, Bajema IM, van der Kooij SW, et al. Quantification of dendritic cell subsets in human renal tissue under normal and pathological conditions. Kidney Int. 2007;71(10):1001–8. https://doi.org/10.1038/sj.ki.5002187.

    Article  CAS  PubMed  Google Scholar 

  48. Kurts C, Panzer U, Anders HJ, Rees AJ. The immune system and kidney disease: basic concepts and clinical implications. Nat Rev Immunol. 2013;13(10):738–53. https://doi.org/10.1038/nri3523.

    Article  CAS  PubMed  Google Scholar 

  49. Lukacs-Kornek V, Burgdorf S, Diehl L, Specht S, Kornek M, Kurts C. The kidney-renal lymph node-system contributes to cross-tolerance against innocuous circulating antigen. J Immunol. 2008;180(2):706–15.

    Article  CAS  PubMed  Google Scholar 

  50. Zewinger S, Schumann T, Fliser D, Speer T. Innate immunity in CKD-associated vascular diseases. Nephrol Dial Transplant. 2016;31(11):1813–21. https://doi.org/10.1093/ndt/gfv358.

    Article  CAS  PubMed  Google Scholar 

  51. Xi Y, Shao F, Bai XY, Cai G, Lv Y, Chen X. Changes in the expression of the toll-like receptor system in the aging rat kidneys. PLoS One. 2014;9(5):e96351. https://doi.org/10.1371/journal.pone.0096351.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Gill PS, Wilcox CS. NADPH oxidases in the kidney. Antioxid Redox Signal. 2006;8(9–10):1597–607. https://doi.org/10.1089/ars.2006.8.1597.

    Article  CAS  PubMed  Google Scholar 

  53. Chang A, Ko K, Clark MR. The emerging role of the inflammasome in kidney diseases. Curr Opin Nephrol Hypertens. 2014;23(3):204–10. https://doi.org/10.1097/01.mnh.0000444814.49755.90.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Liu J, Kennedy DJ, Yan Y, Shapiro JI. Reactive oxygen species modulation of Na/K-ATPase regulates fibrosis and renal proximal tubular sodium handling. Int J Nephrol. 2012;2012:381320. https://doi.org/10.1155/2012/381320.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Srikanthan K, Shapiro JI, Sodhi K. The role of Na/K-ATPase signaling in oxidative stress related to obesity and cardiovascular disease. Molecules 2016;21(9). doi:https://doi.org/10.3390/molecules21091172.

    Article  PubMed Central  Google Scholar 

  56. Xiao J, Zhang X, Fu C, Yang Q, Xie Y, Zhang Z, et al. Impaired Na(+)-K(+)-ATPase signaling in renal proximal tubule contributes to hyperuricemia-induced renal tubular injury. Exp Mol Med. 2018;50(3):e452. https://doi.org/10.1038/emm.2017.287.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. • Sharma K, Karl B, Mathew AV, Gangoiti JA, Wassel CL, Saito R, et al. Metabolomics reveals signature of mitochondrial dysfunction in diabetic kidney disease. J Am Soc Nephrol. 2013;24(11):1901–12. https://doi.org/10.1681/ASN.2013020126. This work presents a metabolomic analysis showing alteration in cellular energetic metabolism during CKD.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Yu B, Zheng Y, Nettleton JA, Alexander D, Coresh J, Boerwinkle E. Serum metabolomic profiling and incident CKD among African Americans. Clin J Am Soc Nephrol. 2014;9(8):1410–7. https://doi.org/10.2215/CJN.11971113.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Darshi M, Van Espen B, Sharma K. Metabolomics in diabetic kidney disease: unraveling the biochemistry of a silent killer. Am J Nephrol. 2016;44(2):92–103. https://doi.org/10.1159/000447954.

    Article  CAS  PubMed  Google Scholar 

  60. Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity. 2014;40(6):833–42. https://doi.org/10.1016/j.immuni.2014.05.014.

    Article  CAS  PubMed  Google Scholar 

  61. Vinolo MA, Ferguson GJ, Kulkarni S, Damoulakis G, Anderson K, Bohlooly YM, et al. SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor. PLoS One. 2011;6(6):e21205. https://doi.org/10.1371/journal.pone.0021205.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Pluznick JL. Gut microbiota in renal physiology: focus on short-chain fatty acids and their receptors. Kidney Int. 2016;90(6):1191–8. https://doi.org/10.1016/j.kint.2016.06.033.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Xiang FF, Zhu JM, Cao XS, Shen B, Zou JZ, Liu ZH, et al. Lymphocyte depletion and subset alteration correlate to renal function in chronic kidney disease patients. Ren Fail. 2016;38(1):7–14. https://doi.org/10.3109/0886022X.2015.1106871.

    Article  PubMed  Google Scholar 

  64. Fadini GP, Rigato M, Cappellari R, Bonora BM, Avogaro A. Long-term prediction of cardiovascular outcomes by circulating CD34+ and CD34+CD133+ stem cells in patients with type 2 diabetes. Diabetes Care. 2017;40(1):125–31. https://doi.org/10.2337/dc16-1755.

    Article  CAS  PubMed  Google Scholar 

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Author notes

  1. Fabrizia Bonacina and Andrea Baragetti contributed equally to this work.

Authors and Affiliations

  1. Department of Excellence of Pharmacological and Biomolecular Sciences (DisFeB), Università Degli Studi di Milano, Via Balzaretti 9, 20133, Milan, Italy

    Fabrizia Bonacina, Andrea Baragetti, Alberico Luigi Catapano & Giuseppe Danilo Norata

  2. SISA Centre, Bassini Hospital, 20092, Cinisello Balsamo, Italy

    Andrea Baragetti & Giuseppe Danilo Norata

  3. IRCSS Multimedica, 20138, Milan, Italy

    Alberico Luigi Catapano

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  1. Fabrizia Bonacina
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  4. Giuseppe Danilo Norata
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Correspondence to Giuseppe Danilo Norata.

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Conflict of Interest

Fabrizia Bonacina and Andrea Baragetti declare that they have no conflict of interest.

Alberico Luigi Catapano reports grants from Sanofi, Amgen. He reports speaker fees from AstraZeneca, Genzyme, Bayer, SigmaTau, Menarini, Kowa, Eli Lilly, Recordati, Pfizer, Sanofi, Mediolanum, Pfizer, Merck, Sanofi, Aegerion, and Amgen.

Giuseppe Danilo Norata reports grants from Pfizer and Amgen, and speaker fees from Sanofi, Aegerion, Amgen, Alnylam, and Novartis.

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Bonacina, F., Baragetti, A., Catapano, A.L. et al. The Interconnection Between Immuno-Metabolism, Diabetes, and CKD. Curr Diab Rep 19, 21 (2019). https://doi.org/10.1007/s11892-019-1143-4

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