Renal FcRn reclaims albumin but facilitates elimination of IgG

Journal of the American Society of Nephrology

Volumn 20, Issue 9, 2009, Pages 1941-1952

  Sarav, Menaka ^a   Wang, Ying ^a   Hack, Bradley K ^a   Chang, Anthony ^a   Jensen, Mark ^a   Bao, Lihua ^a   Quigg, Richard J ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; FC RECEPTOR; IMMUNOGLOBULIN G; SERUM ALBUMIN;

ALBUMIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; DISEASE COURSE; GLOMERULUS FILTRATION; HYPOALBUMINEMIA; KIDNEY; KIDNEY FUNCTION; KIDNEY METABOLISM; KIDNEY TRANSPLANTATION; KIDNEY TUBULE EPITHELIUM; MALE; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; URINARY EXCRETION; WILD TYPE;

ALBUMINURIA; ANIMALS; FEMALE; FLUORESCENT DYES; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNOGLOBULIN G; KIDNEY; KIDNEY TRANSPLANTATION; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROVILLI; MODELS, BIOLOGICAL; ORGANIC CHEMICALS; PODOCYTES; RECEPTORS, FC; SERUM ALBUMIN;

EID: 69849108449     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2008090976     Document Type: Article

References (50)

1. Simister NE, Mostov KE: An Fc receptor structurally related to MHC class I antigens. Nature 337: 184-187, 1989 (Pubitemid 19025381)
2. Simister NE, Story CM, Chen HL, Hunt JS: An IgG-transporting Fc receptor expressed in the syncytiotrophoblast of human placenta. Eur J Immunol 26: 1527-1531, 1996 (Pubitemid 26229998)
3. Simister NE, Rees AR: Isolation and characterization of an Fc receptor from neonatal rat small intestine. Eur J Immunol 15: 733-738, 1985 (Pubitemid 15028949)
4. Borvak J, Richardson J, Medesan C, Antohe F, Radu C, Simionescu M, Ghetie V, Ward ES: Functional expression of the MHC class I-related receptor, FcRn, in endothelial cells of mice. Int Immunol 10: 1289-1298, 1998 (Pubitemid 28414334)
5. Blumberg RS, Koss T, Story CM, Barisani D, Polischuk J, Lipin A, Pablo L, Green R, Simister NE: A major histocompatibility complex class I-related Fc receptor for IgG on rat hepatocytes. J Clin Invest 95: 2397-2402, 1995
6. Haymann JP, Levraud JP, Bouet S, Kappes V, Hagege J, Nguyen G, Xu Y, Rondeau E, Sraer JD: Characterization and localization of the neonatal Fc receptor in adult human kidney. J Am Soc Nephrol 11: 632-639, 2000 (Pubitemid 30171872)
7. Jones EA, Waldmann TA: The mechanism of intestinal uptake and transcellular transport of IgG in the neonatal rat. J Clin Invest 51: 2916-2927, 1972
8. Rodewald R: pH-dependent binding of immunoglobulins to intestinal cells of the neonatal rat. J Cell Biol 71: 666-669, 1976
9. Chaudhury C, Brooks CL, Carter DC, Robinson JM, Anderson CL: Albumin binding to FcRn: Distinct from the FcRn-IgG interaction. Biochemistry 45: 4983-4990, 2006
10. Ward ES, Zhou J, Ghetie V, Ober RJ: Evidence to support the cellular mechanism involved in serum IgG homeostasis in humans. Int Immunol 15: 187-195, 2003 (Pubitemid 36267110)
11. Roopenian DC, Christianson GJ, Sproule TJ, Brown AC, Akilesh S, Jung N, Petkova S, Avanessian L, Choi EY, Shaffer DJ, Eden PA, Anderson CL: The MHC class I-like IgG receptor controls perinatal IgG transport, IgG homeostasis, and fate of IgG-Fc-coupled drugs. J Immunol 170: 3528-3533, 2003 (Pubitemid 36359219)
12. Chaudhury C, Mehnaz S, Robinson JM, Hayton WL, Pearl DK, Roopenian DC, Anderson CL: The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J Exp Med 197: 315-322, 2003 (Pubitemid 36184238)
13. Tryggvason K, Wartiovaara J: How does the kidney filter plasma? Physiology (Bethesda ) 20: 96-101, 2005 (Pubitemid 40627550)
14. Russo LM, Sandoval RM, McKee M, Osicka TM, Collins AB, Brown D, Molitoris BA, Comper WD: The normal kidney filters nephrotic levels of albumin retrieved by proximal tubule cells: Retrieval is disrupted in nephrotic states. Kidney Int 71: 504-513, 2007 (Pubitemid 46398675)
15. Kobayashi N, Suzuki Y, Tsuge T, Okumura K, Ra C, Tomino Y: FcRn-mediated transcytosis of immunoglobulin G in human renal proximal tubular epithelial cells. Am J Physiol Renal Physiol 282: F358-F365, 2002 (Pubitemid 34654568)
16. Akilesh S, Huber TB, Wu H, Wang G, Hartleben B, Kopp JB, Miner JH, Roopenian DC, Unanue ER, Shaw AS: Podocytes use FcRn to clear IgG from the glomerular basement membrane. Proc Natl Acad Sci U S A 105: 967-972, 2008 (Pubitemid 351282065)
17. Hilliard LM, Osicka TM, Clavant SP, Robinson PJ, Nikolic-Paterson DJ, Comper WD: Characterization of the urinary albumin degradation pathway in the isolated perfused rat kidney. J Lab Clin Med 147: 36-44, 2006
18. Roopenian DC, Akilesh S: FcRn: The neonatal Fc receptor comes of age. Nat Rev Immunol 7: 715-725, 2007
19. Israel EJ, Taylor S, Wu Z, Mizoguchi E, Blumberg RS, Bhan A, Simister NE: Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 92: 69-74, 1997 (Pubitemid 27380883)
20. Israel EJ, Wilsker DF, Hayes KC, Schoenfeld D, Simister NE: Increased clearance of IgG in mice that lack beta 2-microglobulin: Possible protective role of FcRn. Immunology 89: 573-578, 1996 (Pubitemid 26419660)
21. Ward ES, Martinez C, Vaccaro C, Zhou J, Tang Q, Ober RJ: From sorting endosomes to exocytosis: Association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol Biol Cell 16: 2028-2038, 2005 (Pubitemid 40471968)
22. Petkova SB, Akilesh S, Sproule TJ, Christianson GJ, Al KH, Brown AC, Presta LG, Meng YG, Roopenian DC: Enhanced half-life of genetically engineered human IgG1 antibodies in a humanized FcRn mouse model: Potential application in humorally mediated autoimmune disease. Int Immunol 18: 1759-1769, 2006 (Pubitemid 44884038)
23. Kim J, Bronson CL, Hayton WL, Radmacher MD, Roopenian DC, Robinson JM, Anderson CL: Albumin turnover: FcRn-mediated recycling saves as much albumin from degradation as the liver produces. Am J Physiol Gastrointest Liver Physiol 290: G352-G360, 2006
24. Bertolatus JA, Hunsicker LG: Glomerular sieving of anionic and neutral bovine albumins in proteinuric rats. Kidney Int 28: 467-476, 1985
25. Tay M, Comper WD, Singh AK: Charge selectivity in kidney ultrafiltration is associated with glomerular uptake of transport probes. Am J Physiol 260: F549-F554, 1991
26. Yu W, Sandoval RM, Molitoris BA: Rapid determination of renal filtration function using an optical ratiometric imaging approach. Am J Physiol Renal Physiol 292: F1873-F1880, 2007
27. Schaeffer RC Jr, Gratrix ML, Mucha DR, Carbajal JM: The rat glomerular filtration barrier does not show negative charge selectivity. Microcirculation 9: 329-342, 2002
28. Birn H, Christensen EI: Renal albumin absorption in physiology and pathology. Kidney Int 69: 440-449, 2006 (Pubitemid 43164434)
29. Eppel GA, Osicka TM, Pratt LM, Jablonski P, Howden B, Glasgow EF, Comper WD: The return of glomerular filtered albumin to the rat renal vein: The albumin retrieval pathway. Ren Fail 23: 347-363, 2001 (Pubitemid 32692271)
30. Koltun M, Comper WD: Retention of albumin in the circulation is governed by saturable renal cell-mediated processes. Microcirculation 11: 351-360, 2004 (Pubitemid 39619085)
31. Koltun M, Nikolovski J, Strong K, Nikolic-Paterson D, Comper WD: Mechanism of hypoalbuminemia in rodents. Am J Physiol Heart Circ Physiol 288: H1604-H1610, 2005
32. Osicka TM, Strong KJ, Nikolic-Paterson DJ, Atkins RC, Jerums G, Comper WD: Renal processing of serum proteins in an albumin-deficient environment: An in vivo study of glomerulonephritis in the Nagase analbuminaemic rat. Nephrol Dial Transplant 19: 320-328, 2004 (Pubitemid 38195979)
33. Greive KA, Nikolic-Paterson DJ, Guimaraes MA, Nikolovski J, Pratt LM, Mu W, Atkins RC, Comper WD: Glomerular permselectivity factors are not responsible for the increase in fractional clearance of albumin in rat glomerulonephritis. Am J Pathol 159: 1159-1170, 2001 (Pubitemid 32847207)
34. Russo LM, Bakris GL, Comper WD: Renal handling of albumin: A critical review of basic concepts and perspective. Am J Kidney Dis 39: 899-919, 2002
35. Mancilla-Jimenez R, Appay MD, Bellon B, Kuhn J, Bariety J, Druet P: IgG Fc membrane receptor on normal human glomerular visceral epithelial cells. Virchows Arch A Pathol Anat Histopathol 404: 139-158, 1984 (Pubitemid 14028687)
36. Michael AF Jr, Drummond KN, Good RA, Vernier RL: Acute poststreptococcal glomerulonephritis: Immune deposit disease. J Clin Invest 45: 237-248, 1966
37. Couser WG, Abrass CK: Pathogenesis of membranous nephropathy. Annu Rev Med 39: 517-530, 1988
38. Kazatchkine MD, Fearon DT, Appay MD, Mandet C, Bariety J: Immunohistochemical study of the human glomerular C3b receptor in normal kidney and in seventy-five cases of renal diseases. J Clin Invest 69: 900-912, 1982
39. Alexander JJ, Wang Y, Chang A, Jacob A, Minto AW, Karmegam M, Haas M, Quigg RJ: Mouse podocyte complement factor H: The functional analogue to human complement receptor 1. J Am Soc Nephrol 18: 1157-1166, 2007 (Pubitemid 46536902)
40. Reiser J, von GG, Loos M, Oh J, Asanuma K, Giardino L, Rastaldi MP, Calvaresi N, Watanabe H, Schwarz K, Faul C, Kretzler M, Davidson A, Sugimoto H, Kalluri R, Sharpe AH, Kreidberg JA, Mundel P: Induction of B7-1 in podocytes is associated with nephrotic syndrome. J Clin Invest 113: 1390-1397, 2004 (Pubitemid 39071694)
41. Schiffer M, Mundel P, Shaw AS, Bottinger EP: A novel role for the adaptor molecule CD2-associated protein in transforming growth factor-beta-induced apoptosis. J Biol Chem 279: 37,004-37,012, 2004 (Pubitemid 39129050)
42. Mendrick DL, Kelly DM, Rennke HG: Antigen processing and presentation by glomerular visceral epithelium in vitro. Kidney Int 39: 71-78, 1991
43. Zhu X, Meng G, Dickinson BL, Li X, Mizoguchi E, Miao L, Wang Y, Robert C, Wu B, Smith PD, Lencer WI, Blumberg RS: MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J Immunol 166: 3266-3276, 2001 (Pubitemid 33117326)
44. Bergtold A, Desai DD, Gavhane A, Clynes R: Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23: 503-514, 2005 (Pubitemid 41587890)
45. Soos TJ, Sims TN, Barisoni L, Lin K, Littman DR, Dustin ML, Nelson PJ: CX3CR1+ interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int 70: 591-596, 2006 (Pubitemid 44141588)
46. Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA, Quigg RJ: Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168: 5817-5823, 2002 (Pubitemid 34556169)
47. Cunningham PN, Wang Y, Guo R, He G, Quigg RJ: Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol 172: 2629-2635, 2004 (Pubitemid 38182415)
48. Bao L, Wang Y, Chang A, Minto AW, Zhou J, Kang H, Haas M, Quigg RJ: Unrestricted C3 activation occurs in Crry-deficient kidneys and rapidly leads to chronic renal failure. J Am Soc Nephrol 18: 811-822, 2007 (Pubitemid 46434498)
49. Bao L, Haas M, Boackle SA, Kraus DM, Cunningham PN, Park P, Alexander JJ, Anderson RA, Culhane C, Holers VM, Quigg RJ: Transgenic expression of a soluble complement inhibitor protects against renal disease and promotes survival in MRL/lpr mice. J Immunol 168: 3601-3607, 2002 (Pubitemid 34250431)
50. Quigg RJ, Lim A, Haas M, Alexander JJ, He C, Carroll MC: Immune complex glomerulonephritis in C4- and C3-deficient mice. Kidney Int 53: 320-330, 1998 (Pubitemid 28097849)