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Clinical and Developmental Immunology
Volume 2010, Article ID 418695, 10 pages
http://dx.doi.org/10.1155/2010/418695
Review Article

Effects of Parathyroid Hormone on Immune Function

1Department of Medicine, Staten Island University Hospital, 475 Seaview Avenue, Staten Island, NY 10305, USA
2NYS Institute for Basic Research in Developmental Disabilities, 1050 Forest Hill Road, Staten Island, NY 10314, USA
3Division of Nephrology, Staten Island University Hospital, 475 Seaview Avenue, Staten Island, NY 10305, USA

Received 13 March 2010; Accepted 15 June 2010

Academic Editor: Stuart Berzins

Copyright © 2010 Abdallah Sassine Geara 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. M. J. Sarnak and B. L. Jaber, “Mortality caused by sepsis in patients with end-stage renal disease compared with the general population,” Kidney International, vol. 58, no. 4, pp. 1758–1764, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. P. C. W. van Dijk, K. J. Jager, F. de Charro et al., “Renal replacement therapy in Europe: the results of a collaborative effort by the ERA-EDTA registry and six national or regional registries,” Nephrology Dialysis Transplantation, vol. 16, no. 6, pp. 1120–1129, 2001. View at Google Scholar · View at Scopus
  3. M. Girndt, M. Sester, U. Sester, H. Kaul, and H. Köhler, “Molecular aspects of T- and B-cell function in uremia,” Kidney International, vol. 59, no. 78, pp. S206–S211, 2001. View at Google Scholar · View at Scopus
  4. C. J. Kelly, “T cell function in chronic renal failure and dialysis,” Blood Purification, vol. 12, no. 1, pp. 36–41, 1994. View at Google Scholar · View at Scopus
  5. E. L. Pesanti, “Immunologic defects and vaccination in patients with chronic renal failure,” Infectious Disease Clinics of North America, vol. 15, no. 3, pp. 813–832, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. W. T. London, M. Di Figlia, A. Sutnick, and B. S. Blumberg, “An epidemic of hepatitis in a chronic-hemodialysis unit. Australia antigen and differences in host response,” New England Journal of Medicine, vol. 281, no. 11, pp. 571–578, 1969. View at Google Scholar · View at Scopus
  7. H. Kohler, W. Arnold, G. Renschin, H. H. Dormeyer, and K. H. Meyer zum Büschenfelde, “Active hepatitis B vaccination of dialysis patients and medical staff,” Kidney International, vol. 25, no. 1, pp. 124–128, 1984. View at Google Scholar
  8. P. Rautenberg, I. Teifke, T. Schlegelberger, and U. Ullmann, “Influenza subtype-specific IgA, IgM and IgG responses in patients on hemodialysis after influenza vaccination,” Infection, vol. 16, no. 6, pp. 323–328, 1988. View at Google Scholar · View at Scopus
  9. M. Girndt, M. Pietsch, and H. Kohler, “Tetanus immunization and its association to hepatitis B vaccination in patients with chronic renal failure,” American Journal of Kidney Diseases, vol. 26, no. 3, pp. 454–460, 1995. View at Google Scholar · View at Scopus
  10. E. A. Friedman, M. M. Beyer, S. R. Hirsch, and G. Schiffman, “Intact antibody response to pneumococcal capsular polysaccharides in uremia and diabetes,” Journal of the American Medical Association, vol. 244, no. 20, pp. 2310–2311, 1980. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Chatenoud, B. Dugas, G. Beaurain et al., “Presence of preactivated T cells in hemodialyzed patients: their possible role in altered immunity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 19, pp. 7457–7461, 1986. View at Google Scholar · View at Scopus
  12. S. C. Meuer, M. Hauer, P. Kurz, K.-H. Meyer zum Buschenfelde, and H. Kohler, “Selective blockade of the antigen-receptor-mediated pathway of T cell activation in patients with impaired primary immune responses,” Journal of Clinical Investigation, vol. 80, no. 3, pp. 743–749, 1987. View at Google Scholar · View at Scopus
  13. M. Girndt, H. Kohler, E. Schiedhelm-Weick, J. F. Schlaak, K.-H. Meyer Zum Buschenfelde, and B. Fleischer, “Production of interleukin-6, tumor necrosis factor α and interleukin-10 in vitro correlates with the clinical immune defect in chronic hemodialysis patients,” Kidney International, vol. 47, no. 2, pp. 559–565, 1995. View at Google Scholar · View at Scopus
  14. T. Eleftheriadis, G. Antoniadi, V. Liakopoulos, C. Kartsios, and I. Stefanidis, “Disturbances of acquired immunity in hemodialysis patients,” Seminars in Dialysis, vol. 20, no. 5, pp. 440–451, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. M. Girndt, M. Sester, U. Sester, H. Kaul, and H. Köhler, “Defective expression of B7-2 (CD86) on monocytes of dialysis patients correlates to the uremia-associated immune defect,” Kidney International, vol. 59, no. 4, pp. 1382–1389, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. P. Stenvinkel, O. Heimbürger, B. Lindholm, G. A. Kaysen, and J. Bergström, “Are there two types of malnutrition in chronic renal failure? Evidence for relationships between malnutrition, inflammation and atherosclerosis (MIA syndrome),” Nephrology Dialysis Transplantation, vol. 15, no. 7, pp. 953–960, 2000. View at Google Scholar · View at Scopus
  17. M. Chonchol, “Neutrophil dysfunction and infection risk in end-stage renal disease,” Seminars in Dialysis, vol. 19, no. 4, pp. 291–296, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. R. Shurtz-Swirski, T. Shkolnik, and S. M. Shasha, “Parathyroid hormone and the cellular immune system,” Nephron, vol. 70, no. 1, pp. 21–24, 1995. View at Google Scholar · View at Scopus
  19. D. M. Voss and E. H. Drake, “Cardiac manifestations of hyperparathyroidism, with presentation of a previously unreported arrhythmia,” American Heart Journal, vol. 73, no. 2, pp. 235–239, 1967. View at Google Scholar · View at Scopus
  20. E. Bogin, S. G. Massry, and I. Harary, “Effect of parathyroid hormone on rat heart cells,” Journal of Clinical Investigation, vol. 67, no. 4, pp. 1215–1227, 1981. View at Google Scholar · View at Scopus
  21. G. N. Rizzo and C. W. Olanow, “Neurologic manifestations of hyperparathyroidism. Study of 120 cases,” Arquivos de Neuro-Psiquiatria, vol. 40, no. 3, pp. 213–222, 1982. View at Google Scholar · View at Scopus
  22. D. Myetes, E. Bogin, A. Ma, P. P. Dukes, and S. G. Massry, “Effect of parathyroid hormone on erythropoiesis,” Journal of Clinical Investigation, vol. 67, no. 5, pp. 1263–1269, 1981. View at Google Scholar · View at Scopus
  23. E. Bogin, S. G. Massry, J. Levi, M. Djaldeti, G. Bristol, and J. Smith, “Effect of parathyroid hormone on osmotic fragility of human erythrocytes,” Journal of Clinical Investigation, vol. 69, no. 4, pp. 1017–1025, 1982. View at Google Scholar · View at Scopus
  24. S. Kumar, A. O. Olukoga, C. Gordoni et al., “Impaired glucose tolerance and insulin insensitivity in primary hyperparathyroidism,” Clinical Endocrinology, vol. 40, no. 1, pp. 47–53, 1994. View at Google Scholar · View at Scopus
  25. S. Ayturk, A. Gursoy, N. B. Tutuncu, D. T. Ertugrul, and N. G. Demirag, “Changes in insulin sensitivity and glucose and bone metabolism over time in patients with asymptomatic primary hyperparathyroidism,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 11, pp. 4260–4263, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. L. Kaplan, A. D. Katz, C. Ben-Isaac, and S. G. Massry, “Malignant neoplasms and parathyroid adenoma,” Cancer, vol. 28, no. 2, pp. 401–407, 1971. View at Google Scholar · View at Scopus
  27. J. C. Wang, W. Steier, M. K. Aung, and M. S. Tobin, “Primary hyperparathyroidism and chronic lymphocytic leukemia,” Cancer, vol. 42, no. 4, pp. 1964–1969, 1978. View at Google Scholar · View at Scopus
  28. R. N. Dexter, F. Mullinax, H. L. Estep, and R. C. Williams Jr., “Monoclonal IgG gammopathy and hyperparathyroidism,” Annals of Internal Medicine, vol. 77, no. 5, pp. 759–764, 1972. View at Google Scholar · View at Scopus
  29. H. M. Perry III, J. C. Chappel, E. Bellorin-Font, J. Tamao, K. J. Martin, and S. L. Teitelbaum, “Parathyroid hormone receptors in circulating human mononuclear leukocytes,” Journal of Biological Chemistry, vol. 259, no. 9, pp. 5531–5535, 1984. View at Google Scholar · View at Scopus
  30. H. E. Gruber, “Bone and the immune system,” Proceedings of the Society for Experimental Biology and Medicine, vol. 197, no. 3, pp. 219–225, 1991. View at Google Scholar · View at Scopus
  31. P. Chen, C. Trummel, J. Horton, J. J. Baker, and J. J. Oppenheim, “Production of osteoclast activating factor by normal human peripheral blood rosetting and nonrosetting lymphocytes,” European Journal of Immunology, vol. 6, no. 10, pp. 732–736, 1976. View at Google Scholar · View at Scopus
  32. G. Milhaud and M. L. Labat, “Thymus and osteopetrosis,” Clinical Orthopaedics and Related Research, vol. 135, pp. 260–271, 1978. View at Google Scholar · View at Scopus
  33. T. Yoneda and G. R. Mundy, “Monocytes regulate osteoclast-activating factor production by releasing prostaglandins,” Journal of Experimental Medicine, vol. 150, no. 2, pp. 338–350, 1979. View at Google Scholar · View at Scopus
  34. C. Minkin, L. Blackman, J. Newbrey, S. Pokress, R. Posek, and M. Walling, “Effects of parathyroid hormone and calcitonin on adenylate cyclase in murine mononuclear phagocytes,” Biochemical and Biophysical Research Communications, vol. 76, no. 3, pp. 875–881, 1977. View at Google Scholar · View at Scopus
  35. I. Yamamoto, J. T. Potts Jr., and G. V. Segre, “Circulating bovine lymphocytes contain receptors for parathyroid hormone,” Journal of Clinical Investigation, vol. 71, no. 2, pp. 404–407, 1983. View at Google Scholar · View at Scopus
  36. A. A. Bialasiewicz, H. Jueppner, V. Diehl, and R. D. Hesch, “Binding of bovine parathyroid hormone to surface receptors of cultured B-lymphocytes,” Biochimica et Biophysica Acta, vol. 584, no. 3, pp. 467–478, 1979. View at Google Scholar · View at Scopus
  37. S. M. Shasha, B. Kristal, M. Barzilai, U. E. Makov, and T. Shkolnik, “In vitro effect of PTH on normal T cell functions,” Nephron, vol. 50, no. 3, pp. 212–216, 1988. View at Google Scholar · View at Scopus
  38. J. M. Alexiewicz, M. Klinger, T. O. Pitts, Z. Gaciong, M. Linker-Israeli, and S. G. Massry, “Parathyroid hormone inhibits B cell proliferation: implications in chronic renal failure,” Journal of the American Society of Nephrology, vol. 1, no. 3, pp. 236–244, 1990. View at Google Scholar · View at Scopus
  39. T. Kaneko, E. Osono, N. Hayama, Y. Lino, and A. Terashi, “T-cell activation modified by parathyroid hormone (PTH) in patients with end-stage renal disease,” Clinical Nephrology, vol. 48, no. 6, pp. 353–358, 1997. View at Google Scholar · View at Scopus
  40. M. Klinger, J. M. Alexiewicz, M. Linker-Israeli et al., “Effect of parathyroid hormone on human T cell activation,” Kidney International, vol. 37, no. 6, pp. 1543–1551, 1990. View at Google Scholar · View at Scopus
  41. E. Lewin, J. Ladefoged, L. Brandi, and K. Olgaard, “Parathyroid hormone dependent T cell proliferation in uremic rats,” Kidney International, vol. 44, no. 2, pp. 379–384, 1993. View at Google Scholar · View at Scopus
  42. D. Angelini, A. Carlini, R. Giusti et al., “Parathyroid hormone and T-cellular immunity in uremic patients in replacement dialytic therapy,” Artificial Organs, vol. 17, no. 2, pp. 73–75, 1993. View at Google Scholar
  43. D. Angelini, A. Carlini, L. Mazzotta et al., “Immunologic disturbances and levels of parathyroid hormone in uremic patients in replacement dialysis therapy,” Clinical Nephrology, vol. 42, no. 4, pp. 246–250, 1994. View at Google Scholar
  44. C. Tzanno-Martins, E. Futata, V. Jorgetti, and A. J. S. Duarte, “Restoration of impaired T-cell proliferation after parathyroidectomy in hemodialysis patients,” Nephron, vol. 84, no. 3, pp. 224–227, 2000. View at Google Scholar
  45. F. N. Ozdemir, U. Yakupoglu, M. Turan et al., “Role of parathormone levels on T-cell response in hemodialysis patients,” Transplantation Proceedings, vol. 34, no. 6, pp. 2044–2045, 2002. View at Publisher · View at Google Scholar
  46. S. G. Massry, J. W. Coburn, G. M. Chertow et al., “K/DOQI clinical practice guidelines for bone metabolism and disease in chronic kidney disease,” American Journal of Kidney Diseases, vol. 42, no. 4, pp. S1–S201, 2003. View at Google Scholar
  47. J.-W. Yoon, S. Gollapudi, M. V. Pahl, and N. D. Vaziri, “Naïve and central memory T-cell lymphopenia in end-stage renal disease,” Kidney International, vol. 70, no. 2, pp. 371–376, 2006. View at Publisher · View at Google Scholar · View at PubMed
  48. M. Haag-Weber and W. H. Horl, “The immune system in uremia and during its treatment,” New Horizons, vol. 3, no. 4, pp. 669–679, 1995. View at Google Scholar
  49. J. L. Touraine, F. Touraine, J. P. Revillard, J. Brochier, and J. Traeger, “T lymphocytes and serum inhibitors of cell mediated immunity in renal insufficiency,” Nephron, vol. 14, no. 2, pp. 195–208, 1975. View at Google Scholar
  50. S. M. Shasha, B. Kristal, O. Steinberg, and T. Shkolnik, “Effect of parathyroidectomy on T cell functions in patients with primary hyperparathyroidism,” American Journal of Nephrology, vol. 9, no. 1, pp. 25–29, 1989. View at Google Scholar
  51. Z. Gaciong, J. M. Alexiewicz, and S. G. Massry, “Impaired in vivo antibody production in CRF rats: role of secondary hyperparathyroidism,” Kidney International, vol. 40, no. 5, pp. 862–867, 1991. View at Google Scholar
  52. I. Chervu, M. Kiersztejn, J. M. Alexiewicz, G. Z. Fadda, M. Smogorzewski, and S. G. Massry, “Impaired phagocytosis in chronic renal failure is mediated by secondary hyperparathyroidism,” Kidney International, vol. 41, no. 6, pp. 1501–1505, 1992. View at Google Scholar
  53. H. Kotzmann, M. Köller, C. Abela et al., “Effects of parathyroid hormone and serum calcium on the phenotype and function of mononuclear cells in patients with primary hyperparathyroidism,” European Journal of Clinical Investigation, vol. 28, no. 5, pp. 353–358, 1998. View at Publisher · View at Google Scholar
  54. F. Giacchino, G. Quattrocchio, and G. Piccoli, “Parathyroid hormone as a uremic toxin: its influence on T lymphocyte receptors,” Clinical Nephrology, vol. 23, no. 2, pp. 105–106, 1985. View at Google Scholar
  55. Y. Jiang, A. Yoshida, C. Ishioka, H. Kimata, and H. Mikawa, “Parathyroid hormone inhibits immunoglobulin production without affecting cell growth in human B cells,” Clinical Immunology and Immunopathology, vol. 65, no. 3, pp. 286–293, 1992. View at Publisher · View at Google Scholar
  56. Z. Gaciong, J. M. Alexiewicz, M. Linker-Israeli, I. A. Shulman, T. O. Pitts, and S. G. Massry, “Inhibition of immunoglobulin production by parathyroid hormone. Implications in chronic renal failure,” Kidney International, vol. 40, no. 1, pp. 96–106, 1991. View at Google Scholar
  57. A. B. Hauser, A. E. M. Stinghen, S. Kato et al., “Characteristics and causes of immune dysfunction related to uremia and dialysis,” Peritoneal Dialysis International, vol. 28, no. 3, pp. S183–S187, 2008. View at Google Scholar
  58. G. Cohen, M. Haag-Weber, and W. H. Horl, “Immune dysfunction in uremia,” Kidney International, vol. 51, no. 62, pp. S79–S82, 1997. View at Google Scholar
  59. J. M. Alexiewicz, M. Smogorzewski, M. Klin, M. Akmal, and S. G. Massry, “Effect of treatment of hemodialysis patients with nifedipine on metabolism and function of polymorphonuclear leukocytes,” American Journal of Kidney Diseases, vol. 25, no. 3, pp. 440–444, 1995. View at Google Scholar
  60. J. M. Alexiewicz, M. Smogorzewski, S. K. Gill, M. Akmal, and S. G. Massry, “Time course of the effect of nifedipine therapy and its discontinuation on [Ca2+](i) and phagocytosis of polymorphonuclear leukocytes from hemodialysis patients,” American Journal of Nephrology, vol. 17, no. 1, pp. 12–16, 1997. View at Google Scholar
  61. C. C. Doherty, P. LaBelle, J. F. Collins, N. Brautbar, and S. G. Massry, “Effect of parathyroid hormone in random migration of human polymorphonuclear leukocytes,” American Journal of Nephrology, vol. 8, no. 3, pp. 212–219, 1988. View at Google Scholar
  62. J. M. Alexiewicz, M. Smogorzewski, G. Z. Fadda, and S. G. Massry, “Impaired phagocytosis in dialysis patients: studies on mechanisms,” American Journal of Nephrology, vol. 11, no. 2, pp. 102–111, 1991. View at Google Scholar
  63. D. J. Salant, A. M. Glover, R. Anderson et al., “Polymorphonuclear leucocyte function in chronic renal failure and after renal transplantation,” Proceedings of the European Dialysis and Transplant Association, vol. 12, pp. 370–379, 1976. View at Google Scholar
  64. F. Khan, A. J. Khan, C. Papagaroufalis, J. Warman, P. Khan, and H. E. Evans, “Reversible defect of neutrophil chemotaxis and random migration in primary hyperparathyroidism,” Journal of Clinical Endocrinology and Metabolism, vol. 48, no. 4, pp. 582–584, 1979. View at Google Scholar
  65. S. N. Tuma, R. R. Martin, L. E. Mallette, and G. Eknoyan, “Augmented polymorphonuclear chemiluminescence in patients with secondary hyperparathyroidism,” Journal of Laboratory and Clinical Medicine, vol. 97, no. 2, pp. 291–298, 1981. View at Google Scholar
  66. S. G. Massry, R. M. Schaeffer, M. Teschner, M. Roeder, J. F. Zull, and A. Heidland, “Effect of parathyroid hormone on elastase release from human polymorphonuclear leucocytes,” Kidney International, vol. 36, no. 5, pp. 883–890, 1989. View at Google Scholar
  67. R. Esposito, C. Romano-Carratelli, N. Lanzetti et al., “Toxicity in uremia 2. Correlation between PTH levels and impaired aspecific immunity,” International Journal of Artificial Organs, vol. 11, no. 3, pp. 159–160, 1988. View at Google Scholar
  68. W. H. Horl, M. Haag-Weber, B. Mai, and S. G. Massry, “Verapamil reverses abnormal [Ca2+]i and carbohydrate metabolism of PMNL of dialysis patients,” Kidney International, vol. 47, no. 6, pp. 1741–1745, 1995. View at Google Scholar
  69. M. Kiersztejn, M. Smogorzewski, P. Thanakitcharu, G. Z. Fadda, and S. G. Massry, “Decreased O2 consumption by PMNL from humans and rats with CRF: role of secondary hyperparathyroidism,” Kidney International, vol. 42, no. 3, pp. 602–609, 1992. View at Google Scholar
  70. N. Seyrek, W. Marcinkowski, M. Smogorzewski, T. M. Demerdash, and S. G. Massry, “Amlodipine prevents and reverses the elevation in [Ca2+](i) and the impaired phagocytosis of PMNL of diabetic rats,” Nephrology Dialysis Transplantation, vol. 12, no. 2, pp. 265–272, 1997. View at Publisher · View at Google Scholar
  71. M. Haag-Weber, B. Mai, and W. H. Horl, “Effect of hemodialysis on intracellular calcium in human polymorphonuclear neutrophils,” Mineral and Electrolyte Metabolism, vol. 18, no. 2–5, pp. 151–155, 1992. View at Google Scholar
  72. S. G. Massry and G. Z. Fadda, “Chronic renal failure is a state of cellular calcium toxicity,” American Journal of Kidney Diseases, vol. 21, no. 1, pp. 81–86, 1993. View at Google Scholar