Skip to main content
SpringerLink
Log in
Book cover

Biomarkers in Kidney Disease pp 557–575Cite as

BLyS and APRIL Cytokines as Biomarkers of Kidney Diseases

  • Reference work entry
  • First Online:

  • 1357 Accesses

Abstract

Kidney damages mediated by the immune system have been reported for glomerular diseases, tubulointerstitial nephritis, and rejection of the allograft posttransplantation. B-lymphocytes have an important role in the pathogenesis for these kidney diseases. There are increasing evidences that TNF-like ligands which regulate B-cell homeostasis such as B-lymphocyte stimulator (BLyS) and a proliferation-inducing ligand (APRIL) can be used to detect kidney diseases as well as acute rejection of the kidney allograft. This chapter will review these two ligands, BLyS and APRIL, and its promising prospect in detecting glomerular diseases and acute rejection of the kidney allograft.

BLyS and APRIL are found in the plasma and membrane proteins of macrophages, monocytes, and dendritic cells. Both can activate the proliferation of B-cells and plasma cells. They are expressed on tissues of the lymph node, bone marrow, synovium, and kidney. Even though both cytokines share a common receptor on the B-cells, however, their roles in B-cell activation are significantly different. When BLyS is activated, this will result in severe B-cell hyperplasia in BLyS-transgenic mice. In contrast, when APRIL is activated, there is no effect on the homeostasis of the lymphoid in APRIL-transgenic mice.

BLyS was initially discovered to be a potential therapeutic target for lupus patients. Later, it was shown that both BLyS and APRIL were somehow associated with lupus nephritis. Both cytokines are expressed on the infiltrating monocytes and/or macrophages of patients with lupus nephritis. It remains unknown whether the blockade of both cytokines can be used to treat the lupus disease. However, serum APRIL has been shown to be a useful biomarker in detecting lupus nephritis in patients with a poor prognosis.

In kidney transplantation, B-cell is an important factor for the long-term survival of the kidney allograft. High levels of BLyS or APRIL can activate alloreactive B-cells by inducing antibodies against the donor antigens (donor-specific antibody, DSA) and result in rejection of the allograft. Aside from that, BLyS is an important growth factor for IL-10-producing B-cells known as the regulatory B-cells. It has been shown that BLyS from the mice can increase a proportion of regulatory B-cells ex vivo. These evidences indicate that BLyS plays a major role in the activation and regulation of the immune system affecting the success and/or outcome of the kidney transplantation.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   449.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

ABMR:

Antibody-mediated rejection

AKD:

Acute kidney disease

APRIL:

A proliferation-inducing ligand

BAFF:

B-cell-activating factor

BAFF-R:

B-cell-activating factor receptor

BCMA:

B-cell maturation antigen

BCR:

B-cell receptor

BLyS:

B-lymphocyte stimulator

CD:

Cluster of differentiation

CKD:

Chronic kidney disease

CR:

Complement receptor

Cr:

Creatinine

DSA:

Donor-specific antibody

GFR:

Glomerular filtration rate

HLA:

Human leukocyte antigen

IF/TA:

Interstitial fibrosis/tubular atrophy

IL:

Interleukin

NSTDA:

National Science and Technology Development Agency

PLA2R:

M-type phospholipase A2 receptor

SLE:

Systemic lupus erythematosus

suPAR:

Soluble urokinase-type plasminogen activator receptor

TACI:

Transmembrane activator and calcium modulator and cyclophilin ligand interactor

TNF:

Tumor necrosis factor

References

  • Alba P, Bento L, Cuadrado MJ, Karim Y, Tungekar MF, Abbs I, Khamashta MA, D’Cruz D, Hughes GR. Anti-dsDNA, anti-Sm antibodies, and the lupus anticoagulant: significant factors associated with lupus nephritis. Ann Rheum Dis. 2003;62(6):556–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anolik JH, Barnard J, Owen T, Zheng B, Kemshetti S, Looney RJ, Sanz I. Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum. 2007;56(9):3044–56.

    Article  CAS  PubMed  Google Scholar 

  • Arce E, Jackson DG, Gill MA, Bennett LB, Banchereau J, Pascual V. Increased frequency of pre-germinal center B cells and plasma cell precursors in the blood of children with systemic lupus erythematosus. J Immunol. 2001;167(4):2361–9.

    Article  CAS  PubMed  Google Scholar 

  • Banham G, Prezzi D, Harford S, Taylor CJ, Hamer R, Higgins R, Bradley JA, Clatworthy MR. Elevated pretransplantation soluble BAFF is associated with an increased risk of acute antibody-mediated rejection. Transplantation. 2013;96(4):413–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck Jr LH, Bonegio RG, Lambeau G, Beck DM, Powell DW, Cummins TD, Klein JB, Salant DJ. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med. 2009;361(1):11–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belnoue E, Pihlgren M, McGaha TL, Tougne C, Rochat AF, Bossen C, Schneider P, Huard B, Lambert PH, Siegrist CA. APRIL is critical for plasmablast survival in the bone marrow and poorly expressed by early-life bone marrow stromal cells. Blood. 2008;111(5):2755–64.

    Article  CAS  PubMed  Google Scholar 

  • Benson MJ, Dillon SR, Castigli E, Geha RS, Xu S, Lam KP, Noelle RJ. Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J Immunol. 2008;180(6):3655–9.

    Article  CAS  PubMed  Google Scholar 

  • Bloom D, Chang Z, Pauly K, Kwun J, Fechner J, Hayes C, Samaniego M, Knechtle S. BAFF is increased in renal transplant patients following treatment with alemtuzumab. Am J Transplant. 2009;9(8):1835–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bossen C, Cachero TG, Tardivel A, Ingold K, Willen L, Dobles M, Scott ML, Maquelin A, Belnoue E, Siegrist CA, Chevrier S, Acha-Orbea H, Leung H, Mackay F, Tschopp J, Schneider P. TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood. 2008;111(3):1004–12.

    Article  CAS  PubMed  Google Scholar 

  • Comoli P, Quartuccio G, Cioni M, Parodi A, Nocera A, Basso S, Fontana I, Magnasco A, Sioli V, Guido I, Klersy C, Zecca M, Cardillo M, Ghiggeri GM, Ginevri F. Posttransplant soluble B-cell activating factor kinetics in pediatric recipients of first kidney allograft. Transplantation. 2015;99(1):243–9.

    Article  CAS  PubMed  Google Scholar 

  • Cortes-Hernandez J, Ordi-Ros J, Labrador M, Bujan S, Balada E, Segarra A, Vilardell-Tarres M. Antihistone and anti-double-stranded deoxyribonucleic acid antibodies are associated with renal disease in systemic lupus erythematosus. Am J Med. 2004;116(3):165–73.

    Article  CAS  PubMed  Google Scholar 

  • Darce JR, Arendt BK, Wu X, Jelinek DF. Regulated expression of BAFF-binding receptors during human B cell differentiation. J Immunol. 2007;179(11):7276–86.

    Article  CAS  PubMed  Google Scholar 

  • Day ES, Cachero TG, Qian F, Sun Y, Wen D, Pelletier M, Hsu YM, Whitty A. Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry. 2005;44(6):1919–31.

    Article  CAS  PubMed  Google Scholar 

  • Dillon SR, Gross JA, Ansell SM, Novak AJ. An APRIL to remember: novel TNF ligands as therapeutic targets. Nat Rev Drug Discov. 2006;5(3):235–46.

    Article  CAS  PubMed  Google Scholar 

  • Doolan PD, Alpen EL, Theil GB. A clinical appraisal of the plasma concentration and endogenous clearance of creatinine. Am J Med. 1962;32:65–79.

    Article  CAS  PubMed  Google Scholar 

  • Eilertsen GO, Nossent JC. APRIL levels strongly correlate with IL-17 in systemic lupus erythematosus. Lupus. 2014;23(13):1383–91.

    Article  CAS  PubMed  Google Scholar 

  • Everly MJ, Rebellato LM, Haisch CE, Ozawa M, Parker K, Briley KP, Catrou PG, Bolin P, Kendrick WT, Kendrick SA, Harland RC, Terasaki PI. Incidence and impact of de novo donor-specific alloantibody in primary renal allografts. Transplantation. 2013;95(3):410–7.

    Article  CAS  PubMed  Google Scholar 

  • Forger F, Matthias T, Oppermann M, Becker H, Helmke K. Clinical significance of anti-dsDNA antibody isotypes: IgG/IgM ratio of anti-dsDNA antibodies as a prognostic marker for lupus nephritis. Lupus. 2004;13(1):36–44.

    Article  CAS  PubMed  Google Scholar 

  • Furie R, Petri M, Zamani O, Cervera R, Wallace DJ, Tegzova D, Sanchez-Guerrero J, Schwarting A, Merrill JT, Chatham WW, Stohl W, Ginzler EM, Hough DR, Zhong ZJ, Freimuth W, van Vollenhoven RF. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 2011;63(12):3918–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorelik L, Cutler AH, Thill G, Miklasz SD, Shea DE, Ambrose C, Bixler SA, Su L, Scott ML, Kalled SL. Cutting edge: BAFF regulates CD21/35 and CD23 expression independent of its B cell survival function. J Immunol. 2004;172(2):762–6.

    Article  CAS  PubMed  Google Scholar 

  • Gras MP, Laabi Y, Linares-Cruz G, Blondel MO, Rigaut JP, Brouet JC, Leca G, Haguenauer-Tsapis R, Tsapis A. BCMAp: an integral membrane protein in the Golgi apparatus of human mature B lymphocytes. Int Immunol. 1995;7(7):1093–106.

    Article  CAS  PubMed  Google Scholar 

  • Groom JR, Fletcher CA, Walters SN, Grey ST, Watt SV, Sweet MJ, Smyth MJ, Mackay CR, Mackay F. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J Exp Med. 2007;204(8):1959–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hildebrand JM, Luo Z, Manske MK, Price-Troska T, Ziesmer SC, Lin W, Hostager BS, Slager SL, Witzig TE, Ansell SM, Cerhan JR, Bishop GA, Novak AJ. A BAFF-R mutation associated with non-Hodgkin lymphoma alters TRAF recruitment and reveals new insights into BAFF-R signaling. J Exp Med. 2010;207(12):2569–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu BL, Harless SM, Lindsley RC, Hilbert DM, Cancro MP. Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J Immunol. 2002;168(12):5993–6.

    Article  CAS  PubMed  Google Scholar 

  • Kappos L, Hartung HP, Freedman MS, Boyko A, Radu EW, Mikol DD, Lamarine M, Hyvert Y, Freudensprung U, Plitz T, van Beek J. Atacicept in multiple sclerosis (ATAMS): a randomised, placebo-controlled, double-blind, phase 2 trial. Lancet Neurol. 2014;13(4):353–63.

    Article  CAS  PubMed  Google Scholar 

  • Kasiske BL, Gaston RS, Gourishankar S, Halloran PF, Matas AJ, Jeffery J, Rush D. Long-term deterioration of kidney allograft function. Am J Transplant. 2005;5(6):1405–14.

    Article  PubMed  Google Scholar 

  • Levey AS. Measurement of renal function in chronic renal disease. Kidney Int. 1990;38(1):167–84.

    Article  CAS  PubMed  Google Scholar 

  • Li F, Zheng C, Zhong Y, Zeng C, Xu F, Yin R, Jiang Q, Zhou M, Liu Z. Relationship between serum soluble urokinase plasminogen activator receptor level and steroid responsiveness in FSGS. Clin J Am Soc Nephrol. 2014;9(11):1903–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Zou Y, Davidson A. Plasma cells in systemic lupus erythematosus: the long and short of it all. Eur J Immunol. 2011;41(3):588–91.

    Article  CAS  PubMed  Google Scholar 

  • Mackay F, Leung H. The role of the BAFF/APRIL system on T cell function. Semin Immunol. 2006;18(5):284–9.

    Article  CAS  PubMed  Google Scholar 

  • Mackay F, Schneider P. TACI, an enigmatic BAFF/APRIL receptor, with new unappreciated biochemical and biological properties. Cytokine Growth Factor Rev. 2008;19(3–4):263–76.

    Article  CAS  PubMed  Google Scholar 

  • Mackay F, Schneider P. Cracking the BAFF code. Nat Rev Immunol. 2009;9(7):491–502.

    Article  CAS  PubMed  Google Scholar 

  • Mackay F, Schneider P, Rennert P, Browning J. BAFF AND APRIL: a tutorial on B cell survival. Annu Rev Immunol. 2003;21:231–64.

    Article  CAS  PubMed  Google Scholar 

  • Mackay F, Sierro F, Grey ST, Gordon TP. The BAFF/APRIL system: an important player in systemic rheumatic diseases. Curr Dir Autoimmun. 2005;8:243–65.

    Article  CAS  PubMed  Google Scholar 

  • Marsters SA, Yan M, Pitti RM, Haas PE, Dixit VM, Ashkenazi A. Interaction of the TNF homologues BLyS and APRIL with the TNF receptor homologues BCMA and TACI. Curr Biol. 2000;10(13):785–8.

    Article  CAS  PubMed  Google Scholar 

  • Merrill JT, Burgos-Vargas R, Westhovens R, Chalmers A, D’Cruz D, Wallace DJ, Bae SC, Sigal L, Becker JC, Kelly S, Raghupathi K, Li T, Peng Y, Kinaszczuk M, Nash P. The efficacy and safety of abatacept in patients with non-life-threatening manifestations of systemic lupus erythematosus: results of a twelve-month, multicenter, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2010;62(10):3077–87.

    Article  CAS  PubMed  Google Scholar 

  • Meyer-Bahlburg A, Andrews SF, Yu KO, Porcelli SA, Rawlings DJ. Characterization of a late transitional B cell population highly sensitive to BAFF-mediated homeostatic proliferation. J Exp Med. 2008;205(1):155–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morimoto S, Nakano S, Watanabe T, Tamayama Y, Mitsuo A, Nakiri Y, Suzuki J, Nozawa K, Amano H, Tokano Y, Kobata T, Takasaki Y. Expression of B-cell activating factor of the tumour necrosis factor family (BAFF) in T cells in active systemic lupus erythematosus: the role of BAFF in T cell-dependent B cell pathogenic autoantibody production. Rheumatology (Oxford). 2007;46(7):1083–6.

    Article  CAS  Google Scholar 

  • O’Connor BP, Raman VS, Erickson LD, Cook WJ, Weaver LK, Ahonen C, Lin LL, Mantchev GT, Bram RJ, Noelle RJ. BCMA is essential for the survival of long-lived bone marrow plasma cells. J Exp Med. 2004;199(1):91–8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Odendahl M, Jacobi A, Hansen A, Feist E, Hiepe F, Burmester GR, Lipsky PE, Radbruch A, Dorner T. Disturbed peripheral B lymphocyte homeostasis in systemic lupus erythematosus. J Immunol. 2000;165(10):5970–9.

    Article  CAS  PubMed  Google Scholar 

  • Parsons RF, Vivek K, Redfield RR, Migone TS, Cancro MP, Naji A, Noorchashm H. B-cell tolerance in transplantation: is repertoire remodeling the answer? Expert Rev Clin Immunol. 2009;5(6):703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redfield 3rd RR, Rodriguez E, Parsons R, Vivek K, Mustafa MM, Noorchashm H, Naji A. Essential role for B cells in transplantation tolerance. Curr Opin Immunol. 2011;23(5):685–91.

    Article  CAS  PubMed  Google Scholar 

  • Rovin BH, Furie R, Latinis K, Looney RJ, Fervenza FC, Sanchez-Guerrero J, Maciuca R, Zhang D, Garg JP, Brunetta P, Appel G. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 2012;64(4):1215–26.

    Article  CAS  PubMed  Google Scholar 

  • Sfikakis PP, Boletis JN, Lionaki S, Vigklis V, Fragiadaki KG, Iniotaki A, Moutsopoulos HM. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down-regulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum. 2005;52(2):501–13.

    Article  CAS  PubMed  Google Scholar 

  • Shemesh O, Golbetz H, Kriss JP, Myers BD. Limitations of creatinine as a filtration marker in glomerulopathic patients. Kidney Int. 1985;28(5):830–8.

    Article  CAS  PubMed  Google Scholar 

  • Shulga-Morskaya S, Dobles M, Walsh ME, Ng LG, MacKay F, Rao SP, Kalled SL, Scott ML. B cell-activating factor belonging to the TNF family acts through separate receptors to support B cell survival and T cell-independent antibody formation. J Immunol. 2004;173(4):2331–41.

    Article  CAS  PubMed  Google Scholar 

  • Snanoudj R, Candon S, Roelen DL, Jais JP, Claas FH, Legendre C, Chatenoud L. Peripheral B-cell phenotype and BAFF levels are associated with HLA immunization in patients awaiting kidney transplantation. Transplantation. 2014;97(9):917–24.

    Article  CAS  PubMed  Google Scholar 

  • Stadanlick JE, Kaileh M, Karnell FG, Scholz JL, Miller JP, Quinn 3rd WJ, Brezski RJ, Treml LS, Jordan KA, Monroe JG, Sen R, Cancro MP. Tonic B cell antigen receptor signals supply an NF-kappaB substrate for prosurvival BLyS signaling. Nat Immunol. 2008;9(12):1379–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevens LA, Levey AS. Measured GFR as a confirmatory test for estimated GFR. J Am Soc Nephrol. 2009;20(11):2305–13.

    Article  PubMed  Google Scholar 

  • Thibault-Espitia A, Foucher Y, Danger R, Migone T, Pallier A, Castagnet S, G-Gueguen C, Devys A, C-Gautier A, Giral M, Soulillou JP, Brouard S. BAFF and BAFF-R levels are associated with risk of long-term kidney graft dysfunction and development of donor-specific antibodies. Am J Transplant. 2012;12(10):2754–62.

    Article  CAS  PubMed  Google Scholar 

  • Treamtrakanpon W, Tantivitayakul P, Benjachat T, Somparn P, Kittikowit W, Eiam-ong S, Leelahavanichkul A, Hirankarn N, Avihingsanon Y. APRIL, a proliferation-inducing ligand, as a potential marker of lupus nephritis. Arthritis Res Ther. 2012;14(6):R252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Acker BA, Koomen GC, Koopman MG, de Waart DR, Arisz L. Creatinine clearance during cimetidine administration for measurement of glomerular filtration rate. Lancet. 1992;340(8831):1326–9.

    Article  PubMed  Google Scholar 

  • Vincent FB, Morand EF, Schneider P, Mackay F. The BAFF/APRIL system in SLE pathogenesis. Nat Rev Rheumatol. 2014;10(6):365–73.

    Article  CAS  PubMed  Google Scholar 

  • Wei C, Trachtman H, Li J, Dong C, Friedman AL, Gassman JJ, McMahan JL, Radeva M, Heil KM, Trautmann A, Anarat A, Emre S, Ghiggeri GM, Ozaltin F, Haffner D, Gipson DS, Kaskel F, Fischer DC, Schaefer F, Reiser J. Circulating suPAR in two cohorts of primary FSGS. J Am Soc Nephrol. 2012;23(12):2051–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiebe C, Nickerson P. Posttransplant monitoring of de novo human leukocyte antigen donor-specific antibodies in kidney transplantation. Curr Opin Organ Transplant. 2013;18(4):470–7.

    Article  CAS  PubMed  Google Scholar 

  • Wilde B, Thewissen M, Damoiseaux J, Knippenberg S, Hilhorst M, van Paassen P, Witzke O, Cohen Tervaert JW. Regulatory B cells in ANCA-associated vasculitis. Ann Rheum Dis. 2013;72(8):1416–9.

    Article  CAS  PubMed  Google Scholar 

  • Wu P, Everly MJ, Rebellato LM, Haisch CE, Briley KP, Bolin P, Kendrick WT, Kendrick SA, Morgan C, Harland RC, Terasaki PI. Trends and characteristics in early glomerular filtration rate decline after posttransplantation alloantibody appearance. Transplantation. 2013;96(10):919–25.

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Lam KP. B-cell maturation protein, which binds the tumor necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses. Mol Cell Biol. 2001;21(12):4067–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, He X, Sun J, Shi D, Zhu Y, Zhang X. The expression of B-cell activating factor belonging to tumor necrosis factor superfamily (BAFF) significantly correlated with C4D in kidney allograft rejection. Transplant Proc. 2009;41(1):112–6.

    Article  CAS  PubMed  Google Scholar 

  • Yamagata K, Yamagata Y, Kobayashi M, Koyama A. A long-term follow-up study of asymptomatic hematuria and/or proteinuria in adults. Clin Nephrol. 1996;45(5):281–8.

    CAS  PubMed  Google Scholar 

  • Yang M, Sun L, Wang S, Ko KH, Xu H, Zheng BJ, Cao X, Lu L. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J Immunol. 2010;184(7):3321–5.

    Article  CAS  PubMed  Google Scholar 

  • Ye Q, Wang L, Wells AD, Tao R, Han R, Davidson A, Scott ML, Hancock WW. BAFF binding to T cell-expressed BAFF-R costimulates T cell proliferation and alloresponses. Eur J Immunol. 2004;34(10):2750–9.

    Article  CAS  PubMed  Google Scholar 

  • Yurasov S, Wardemann H, Hammersen J, Tsuiji M, Meffre E, Pascual V, Nussenzweig MC. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J Exp Med. 2005;201(5):703–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarkhin V, Li L, Sarwal MM. BAFF may modulate the rate of B-cell repopulation after rituximab therapy for acute renal transplant rejection. Transplantation. 2009;88(10):1229–30.

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

This work is supported by the National Science and Technology Development Agency (NSTDA), Thailand (P-13-00505).

Author information

Authors and Affiliations

  1. Division of Nephrology, Department of Medicine, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial Hospital, Rama4, Pathumwan, 10330, Bangkok, Thailand

    Natavudh Townamchai, Wannarat Pongpirul & Yingyos Avihingsanon

  2. Division of Immunology, Department of Microbiology, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

    Asada Leelahavanichakul

  3. Center of Excellence in Immunology and Immune-Mediated Diseases, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

    Asada Leelahavanichakul & Yingyos Avihingsanon

  4. Department of Medicine, Bamrasnaradura Infectious Diseases Institute, Ministry of Public Health, Tiwanon Rd, 11000, Nonthaburi, Thailand

    Wannarat Pongpirul

Authors
  1. Natavudh Townamchai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wannarat Pongpirul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asada Leelahavanichakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yingyos Avihingsanon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yingyos Avihingsanon .

Editor information

Editors and Affiliations

  1. DeptofBiomedlSci,FacltyofSci&Technology, University of Westminster , London, United Kingdom

    Vinood B. Patel

  2. Department of Nutrition and Dietetics,Division of Diabetes and Nutritional Sciences, Faculty of Life Science and Medicine, King’s College London, London, United Kingdom

    Victor R. Preedy

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this entry

Cite this entry

Townamchai, N., Pongpirul, W., Leelahavanichakul, A., Avihingsanon, Y. (2016). BLyS and APRIL Cytokines as Biomarkers of Kidney Diseases. In: Patel, V., Preedy, V. (eds) Biomarkers in Kidney Disease. Biomarkers in Disease: Methods, Discoveries and Applications. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7699-9_48

Download citation

Publish with us

Policies and ethics

Search

Navigation