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Journal of Diabetes Research
Volume 2016 (2016), Article ID 3486727, 10 pages
http://dx.doi.org/10.1155/2016/3486727
Research Article

An Immunomodulatory Device Improves Insulin Resistance in Obese Porcine Model of Metabolic Syndrome

1Innovative BioTherapies, Inc., 650 Avis Drive, Suite 300, Ann Arbor, MI 48108, USA
2Department of Internal Medicine, University of Michigan Medical School, 4520C MSRB I, SPC 5651, 1150 W. Medical Center Dr., Ann Arbor, MI 48109, USA

Received 25 May 2016; Accepted 31 July 2016

Academic Editor: Maria Pia Francescato

Copyright © 2016 Angela J. Westover et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. E. Kahn, R. L. Hull, and K. M. Utzschneider, “Mechanisms linking obesity to insulin resistance and type 2 diabetes,” Nature, vol. 444, no. 7121, pp. 840–846, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. J. I. Odegaard and A. Chawla, “Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis,” Science, vol. 339, no. 6116, pp. 172–177, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Olefsky and C. K. Glass, “Macrophages, inflammation, and insulin resistance,” Annual Review of Physiology, vol. 72, pp. 219–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Osborn and J. M. Olefsky, “The cellular and signaling networks linking the immune system and metabolism in disease,” Nature Medicine, vol. 18, no. 3, pp. 363–374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. F.-M. Chung, J. C.-R. Tsai, D.-M. Chang, S.-J. Shin, and Y.-J. Lee, “Peripheral total and differential leukocyte count in diabetic nephropathy: the relationship of plasma leptin to leukocytosis,” Diabetes Care, vol. 28, no. 7, pp. 1710–1717, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. W. S. Shim, H. J. Kim, E. S. Kang et al., “The association of total and differential white blood cell count with metabolic syndrome in type 2 diabetic patients,” Diabetes Research and Clinical Practice, vol. 73, no. 3, pp. 284–291, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. C.-R. Tsai, S.-H. Sheu, H.-C. Chiu et al., “Association of peripheral total and differential leukocyte counts with metabolic syndrome and risk of ischemic cardiovascular diseases in patients with type 2 diabetes mellitus,” Diabetes/Metabolism Research and Reviews, vol. 23, no. 2, pp. 111–118, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Nijhuis, S. S. Rensen, Y. Slaats, F. M. H. Van Dielen, W. A. Buurman, and J. W. M. Greve, “Neutrophil activation in morbid obesity, chronic activation of acute inflammation,” Obesity, vol. 17, no. 11, pp. 2014–2018, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Schroder, W. Palinski, and G. W. Schmid-Schonbein, “Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy,” American Journal of Pathology, vol. 139, no. 1, pp. 81–100, 1991. View at Google Scholar · View at Scopus
  10. A. J. van Oostrom, J. P. van Wijk, T. P. Sijmonsma, T. J. Rabelink, and M. Castro Cabezas, “Increased expression of activation markers on monocytes and neutrophils in type 2 diabetes,” Netherlands Journal of Medicine, vol. 62, no. 9, pp. 320–325, 2004. View at Google Scholar · View at Scopus
  11. B. Wierusz-Wysocka, H. Wysocki, H. Siekierka, A. Wykretowicz, A. Szczepanik, and R. Klimas, “Evidence of polymorphonuclear neutrophils (PMN) activation in patients with insulin-dependent diabetes mellitus,” Journal of Leukocyte Biology, vol. 42, no. 5, pp. 519–523, 1987. View at Google Scholar · View at Scopus
  12. Y. S. Lee, P. Li, J. Y. Huh et al., “Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance,” Diabetes, vol. 60, no. 10, pp. 2474–2483, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Gordon and P. R. Taylor, “Monocyte and macrophage heterogeneity,” Nature Reviews Immunology, vol. 5, no. 12, pp. 953–964, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. C. N. Lumeng, J. L. Bodzin, and A. R. Saltiel, “Obesity induces a phenotypic switch in adipose tissue macrophage polarization,” The Journal of Clinical Investigation, vol. 117, no. 1, pp. 175–184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Italiani and D. Boraschi, “From monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation,” Frontiers in Immunology, vol. 5, article 514, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Barisione, S. Garibaldi, G. Ghigliotti et al., “CD14CD16 monocyte subset levels in heart failure patients,” Disease Markers, vol. 28, no. 2, pp. 115–124, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. W. A. Nockher and J. E. Scherberich, “Expanded CD14+ CD16+ Monocyte subpopulation in patients with acute and chronic infections undergoing hemodialysis,” Infection and Immunity, vol. 66, no. 6, pp. 2782–2790, 1998. View at Google Scholar · View at Scopus
  18. R. Patiño, J. Ibarra, A. Rodriguez et al., “Circulating monocytes in patients with diabetes mellitus, arterial disease, and increased CD14 expression,” The American Journal of Cardiology, vol. 85, no. 11, pp. 1288–1291, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Satoh, A. Shimatsu, A. Himeno et al., “Unbalanced M1/M2 phenotype of peripheral blood monocytes in obese diabetic patients: effect of pioglitazone,” Diabetes Care, vol. 33, no. 1, article e7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. B. J. Wrigley, E. Shantsila, L. D. Tapp, and G. Y. H. Lip, “CD14++CD16+ monocytes in patients with acute ischaemic heart failure,” European Journal of Clinical Investigation, vol. 43, no. 2, pp. 121–130, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Yang, H. Gan, Q. Shen, W. Tang, X. Du, and D. Chen, “Proinflammatory CD14+CD16+ monocytes are associated with microinflammation in patients with type 2 diabetes mellitus and diabetic nephropathy uremia,” Inflammation, vol. 35, no. 1, pp. 388–396, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. G. P. Fadini, S. V. De Kreutzenberg, E. Boscaro et al., “An unbalanced monocyte polarisation in peripheral blood and bone marrow of patients with type 2 diabetes has an impact on microangiopathy,” Diabetologia, vol. 56, no. 8, pp. 1856–1866, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. K. S. Rogacev, S. Seiler, A. M. Zawada et al., “CD14++CD16+ monocytes and cardiovascular outcome in patients with chronic kidney disease,” European Heart Journal, vol. 32, no. 1, pp. 84–92, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. K. S. Rogacev, A. M. Zawada, I. Emrich et al., “Lower Apo A-I and lower HDL-C levels are associated with higher intermediate CD14++CD16+monocyte counts that predict cardiovascular events in chronic kidney disease,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 34, no. 9, pp. 2120–2127, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Cipolletta, K. E. Ryan, E. V. Hanna, and E. R. Trimble, “Activation of peripheral blood CD14+ monocytes occurs in diabetes,” Diabetes, vol. 54, no. 9, pp. 2779–2786, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. C. J. Pino, A. S. Yevzlin, K. Lee et al., “Cell-based approaches for the treatment of systemic inflammation,” Nephrology Dialysis Transplantation, vol. 28, no. 2, pp. 296–302, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. C. J. Pino, A. S. Yevzlin, J. Tumlin, and H. D. Humes, “Cell-based strategies for the treatment of kidney dysfunction: a review,” Blood Purification, vol. 34, no. 2, pp. 117–123, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Ding, J. H. Song, J. Y. Jung et al., “A biomimetic membrane device that modulates the excessive inflammatory response to sepsis,” PLoS ONE, vol. 6, no. 4, Article ID e18584, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. M. C. Dyson, M. Alloosh, J. P. Vuchetich, E. A. Mokelke, and M. Sturek, “Components of metabolic syndrome and coronary artery disease in female Ossabaw swine fed excess atherogenic diet,” Comparative Medicine, vol. 56, no. 1, pp. 35–45, 2006. View at Google Scholar · View at Scopus
  30. Z. P. Neeb, J. M. Edwards, M. Alloosh, X. Long, E. A. Mokelke, and M. Sturek, “Metabolic syndrome and coronary artery disease in Ossabaw compared with Yucatan swine,” Comparative Medicine, vol. 60, no. 4, pp. 300–315, 2010. View at Google Scholar · View at Scopus
  31. M. E. Spurlock and N. K. Gabler, “The development of porcine models of obesity and the metabolic syndrome,” Journal of Nutrition, vol. 138, no. 2, pp. 397–402, 2008. View at Google Scholar · View at Scopus
  32. M. Sturek, J. D. Tune, and M. Alloosh, “Ossabaw Island miniature swine: metabolic syndrome and cardiovascular assessment,” in Swine in the Laboratory: Surgery, Anesthesia, Imaging, and Experimental Techniques, M. M. Swindle and A. C. Smith, Eds., pp. 451–465, CRC Press, Boca Raton, Fla, USA, 3rd edition, 2015. View at Google Scholar
  33. J. G. Sham, V. V. Simianu, A. S. Wright et al., “Evaluating the mechanisms of improved glucose homeostasis after bariatric surgery in ossabaw miniature swine,” Journal of Diabetes Research, vol. 2014, Article ID 526972, 7 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Finn and N. Rebuck, “Measurement of adhesion molecule expression on neutrophils and fixation,” Journal of Immunological Methods, vol. 171, no. 2, pp. 267–268, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Hamblin, M. Taylor, J. Bernhagen et al., “A method of preparing blood leucocytes for flow cytometry which prevents upregulation of leucocyte integrins,” Journal of Immunological Methods, vol. 146, no. 2, pp. 219–228, 1992. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Domínguez, B. Alvarez, F. Alonso et al., “Workshop studies on monoclonal antibodies in the myeloid panel with CD11 specificity,” Veterinary Immunology and Immunopathology, vol. 80, no. 1-2, pp. 111–119, 2001. View at Publisher · View at Google Scholar
  37. K. Haverson, A. Saalmüller, B. Alvarez et al., “Overview of the third international workshop on swine leukocyte differentiation antigens,” Veterinary Immunology and Immunopathology, vol. 80, no. 1-2, pp. 5–23, 2001. View at Publisher · View at Google Scholar
  38. S. B. Brown, K. Bailey, and J. Savill, “Actin is cleaved during constitutive apoptosis,” Biochemical Journal, vol. 323, part 1, pp. 233–237, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Keskin, S. Kurtoglu, M. Kendirci, M. E. Atabek, and C. Yazici, “Homeostasis model assessment is more reliable than the fasting glucose/insulin ratio and quantitative insulin sensitivity check index for assessing insulin resistance among obese children and adolescents,” Pediatrics, vol. 115, no. 4, pp. e500–e503, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Astori, F. Vignati, S. Bardelli et al., “‘In vitro’ and multicolor phenotypic characterization of cell subpopulations identified in fresh human adipose tissue stromal vascular fraction and in the derived mesenchymal stem cells,” Journal of Translational Medicine, vol. 5, article 55, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. N. H. Riordan, T. E. Ichim, W.-P. Min et al., “Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis,” Journal of Translational Medicine, vol. 7, article 29, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. R. J. Faris, R. L. Boddicker, J. Walker-Daniels, J. Li, D. E. Jones, and M. E. Spurlock, “Inflammation in response to n3 fatty acids in a porcine obesity model,” Comparative Medicine, vol. 62, no. 6, pp. 495–503, 2012. View at Google Scholar · View at Scopus
  43. M. E. McDonnell, L. M. Ganley-Leal, A. Mehta et al., “B lymphocytes in human subcutaneous adipose crown-like structures,” Obesity, vol. 20, no. 7, pp. 1372–1378, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. W. T. Cade, “Diabetes-related microvascular and macrovascular diseases in the physical therapy setting,” Physical Therapy, vol. 88, no. 11, pp. 1322–1335, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. H. D. Humes, D. Buffington, A. Westover et al., “Immunomodulation with a selective cytopheretic device (SCD) improves myocardial contractility and renal sodium excretion in a canine model of congestive heart failure,” in Proceedings of the ASN Annual Conference, San Diego, Calif, USA, 2012.
  46. H. D. Humes, D. Buffington, A. Westover, K. Johnston, and P. Smith, “Immunomodulation with a Selective Cytopheretic Device (SCD) reduces injury in a pig model of Intracranial Hemorrhage (ICH),” in Proceedings of the ASN Annual Conference, Fort Lauderdale, Fla, USA, 2013.
  47. H. D. Humes, D. Buffington, A. Westover, P. Smith, and H. N. Sabbah, “Immunomodulation with a Selective Cytopheretic Device (SCD) reduces myocardial infarct size in a canine model of Ischemia-Reperfusion Injury (IRI),” in Proceedings of the ASN Annual Conference, San Diego, Calif, USA, 2013.
  48. C. J. Pino, L. Lou, P. L. Smith et al., “A selective cytopheretic inhibitory device for use during cardiopulmonary bypass surgery,” Perfusion, vol. 27, no. 4, pp. 311–319, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Ding, A. S. Yevzlin, Z. Y. Xu et al., “The effects of a novel therapeutic device on acute kidney injury outcomes in the intensive care unit: a pilot study,” ASAIO Journal, vol. 57, no. 5, pp. 426–432, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. H. D. Humes, J. T. Sobota, F. Ding, and J. H. Song, “A selective cytopheretic inhibitory device to treat the immunological dysregulation of acute and chronic renal failure,” Blood Purification, vol. 29, no. 2, pp. 183–190, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. J. A. Tumlin, L. Chawla, A. J. Tolwani et al., “The effect of the selective Cytopheretic device on acute kidney injury outcomes in the intensive care unit: A Multicenter Pilot Study,” Seminars in Dialysis, vol. 26, no. 5, pp. 616–623, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. J. A. Tumlin, C. M. Galphin, A. J. Tolwani et al., “A multi-center, randomized, controlled, pivotal study to assess the safety and efficacy of a selective cytopheretic device in patients with acute kidney injury,” PLoS ONE, vol. 10, no. 8, Article ID e0132482, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. H. D. Humes, B. Szamosfalvi, A. Westover, D. Buffington, and A. Yevzlin, “Immunomodulatory device promotes a shift of circulating monocytes to a less inflammatory phenotype in chronic hemodialysis patients,” ASAIO Journal, 2016. View at Publisher · View at Google Scholar
  54. O. Varga, M. Harangi, I. A. S. Olsson, and A. K. Hansen, “Contribution of animal models to the understanding of the metabolic syndrome: a systematic overview,” Obesity Reviews, vol. 11, no. 11, pp. 792–807, 2010. View at Publisher · View at Google Scholar · View at Scopus