IgA nephropathy: the lectin pathway and implications for targeted therapy

Abstract

Many patients with immunoglobulin A nephropathy (IgAN) progress to kidney failure even with optimal supportive care. An improved understanding of the pathophysiology of IgAN in recent years has led to the investigation of targeted therapies with acceptable tolerability that may address the underlying causes of IgAN or the pathogenesis of kidney injury. The complement system—particularly the lectin and alternative pathways of complement—has emerged as a key mediator of kidney injury in IgAN and a possible target for investigational therapy. This review will focus on the lectin pathway. The examination of kidney biopsies has consistently shown glomerular deposition of mannan-binding lectin (1 of 6 pattern-recognition molecules that activate the lectin pathway) together with IgA1 in up to 50% of patients with IgAN. Glomerular deposition of pattern-recognition molecules for the lectin pathway is associated with more severe glomerular damage and more severe proteinuria and hematuria. Emerging research suggests that the lectin pathway may also contribute to tubulointerstitial fibrosis in IgAN and that collectin-11 is a key mediator of this association. This review summarizes the growing scientific and clinical evidence supporting the role of the lectin pathway in IgAN and examines the possible therapeutic role of lectin pathway inhibition for these patients. Many patients with immunoglobulin A nephropathy (IgAN) progress to kidney failure even with optimal supportive care. An improved understanding of the pathophysiology of IgAN in recent years has led to the investigation of targeted therapies with acceptable tolerability that may address the underlying causes of IgAN or the pathogenesis of kidney injury. The complement system—particularly the lectin and alternative pathways of complement—has emerged as a key mediator of kidney injury in IgAN and a possible target for investigational therapy. This review will focus on the lectin pathway. The examination of kidney biopsies has consistently shown glomerular deposition of mannan-binding lectin (1 of 6 pattern-recognition molecules that activate the lectin pathway) together with IgA1 in up to 50% of patients with IgAN. Glomerular deposition of pattern-recognition molecules for the lectin pathway is associated with more severe glomerular damage and more severe proteinuria and hematuria. Emerging research suggests that the lectin pathway may also contribute to tubulointerstitial fibrosis in IgAN and that collectin-11 is a key mediator of this association. This review summarizes the growing scientific and clinical evidence supporting the role of the lectin pathway in IgAN and examines the possible therapeutic role of lectin pathway inhibition for these patients. Immunoglobulin A nephropathy (IgAN) is the most commonly occurring glomerular disease, and many patients progress to kidney failure even with optimal supportive care and currently available therapy.1Moriyama T. Tanaka K. Iwasaki C. et al.Prognosis in IgA nephropathy: 30-year analysis of 1,012 patients at a single center in Japan.PLoS One. 2014; 9e91756Crossref Scopus (158) Google Scholar,2Kwon C.S. Daniele P. Forsythe A. Ngai C. A systematic literature review of the epidemiology, health-related quality of life impact, and economic burden of immunoglobulin a nephropathy.J Health Econ Outcomes Res. 2021; 8: 36-45Crossref PubMed Scopus (17) Google Scholar Patients with IgAN and persistent proteinuria (>0.75 g/d) have a high risk of progressive loss of kidney function.3Rovin B.H. Adler S.G. Barratt J. et al.Executive summary of the KDIGO 2021 guideline for the management of glomerular diseases.Kidney Int. 2021; 100: 753-779Abstract Full Text Full Text PDF PubMed Scopus (233) Google Scholar Systemic corticosteroids may temporarily slow the progression of kidney disease in these patients, but the data are not consistent and toxicity remains an issue.3Rovin B.H. Adler S.G. Barratt J. et al.Executive summary of the KDIGO 2021 guideline for the management of glomerular diseases.Kidney Int. 2021; 100: 753-779Abstract Full Text Full Text PDF PubMed Scopus (233) Google Scholar When possible, patients with persistent proteinuria should be considered for participation in a clinical trial, in the hopes of discovering safer, effective therapy.3Rovin B.H. Adler S.G. Barratt J. et al.Executive summary of the KDIGO 2021 guideline for the management of glomerular diseases.Kidney Int. 2021; 100: 753-779Abstract Full Text Full Text PDF PubMed Scopus (233) Google Scholar There is clearly an unmet medical need for additional treatment options to slow or even reverse the loss of kidney function. An improved understanding of the pathophysiology of IgAN in recent years has led to the investigation of targeted therapies with acceptable tolerability that may address the underlying causes of IgAN or the downstream pathogenesis of kidney injury. Activation of the complement system—particularly through the lectin and alternative pathways—has emerged as a key mediator of kidney injury in IgAN, including potential contributions to tubulointerstitial fibrosis, and is an attractive target for investigational therapy. The role of the alternative pathway in the pathophysiology of IgAN has been reviewed extensively elsewhere.4Poppelaars F. Faria B. Schwaeble W. Daha M.R. The contribution of complement to the pathogenesis of IgA nephropathy: are complement-targeted therapies moving from rare disorders to more common diseases?.J Clin Med. 2021; 10: 4715Crossref PubMed Scopus (19) Google Scholar Thus, this review focuses on the growing scientific and clinical evidence supporting the pathophysiologic role of the lectin pathway and the possible therapeutic role of lectin pathway inhibition in IgAN. Recent research has elucidated many aspects of how IgAN develops and how it results in kidney injury, but there is still much that remains to be determined. A “four-hit” process has been postulated for IgAN pathophysiology.5Suzuki H. Kiryluk K. Novak J. et al.The pathophysiology of IgA nephropathy.J Am Soc Nephrol. 2011; 22: 1795-1803Crossref PubMed Scopus (535) Google Scholar,6Tumlin J.A. Madaio M.P. Hennigar R. Idiopathic IgA nephropathy: pathogenesis, histopathology, and therapeutic options.Clin J Am Soc Nephrol. 2007; 2: 1054-1061Crossref PubMed Scopus (68) Google Scholar The first hit is the generation (and increased systemic presence) of IgA1 J. A. disease is more common in patients with IgA nephropathy and progression of a Am Soc Nephrol. 2021; PubMed Scopus Google H. is associated with IgA1 in IgA PubMed Scopus Google J. J. The in IgA Nephrol. PubMed Scopus Google Scholar This is to be the has been as a therapeutic target in J. B.H. et target the to IgA Full Text Full Text PDF PubMed Scopus Google Scholar The hit is the of IgA and K. et IgA1 in of IgA nephropathy patients is in with Int. Full Text PDF PubMed Scopus Google Novak J. et in IgA nephropathy of IgA1 with and Clin PubMed Scopus Google Scholar the IgA1 with or H. Novak J. IgA and in 2021; PubMed Scopus Google B. C. et al.The and of in IgA PubMed Scopus Google Scholar The hit the deposition of these in the glomerular injury the complement to kidney and F. Faria B. Schwaeble W. Daha M.R. The contribution of complement to the pathogenesis of IgA nephropathy: are complement-targeted therapies moving from rare disorders to more common diseases?.J Clin Med. 2021; 10: 4715Crossref PubMed Scopus (19) Google in IgA nephropathy: the role of complement in the pathogenesis, and management of IgA Full Text Full Text PDF PubMed Scopus Google Scholar The complement is a key of and that and fibrosis, and in T. J. and are to tubulointerstitial in PubMed Scopus Google A. et of and fibrosis in Full Text Full Text PDF PubMed Scopus (19) Google et and in IgA nephropathy.J Nephrol. PubMed Scopus Google Barratt J. A. The is in IgA nephropathy and is on the kidney PubMed Scopus Google A. et role of in the of glomerular in IgA nephropathy.J Am Soc Nephrol. PubMed Scopus (19) Google T. J. in IgA Nephrol. PubMed Scopus Google P. A. et tubulointerstitial Am Soc Nephrol. 2007; PubMed Scopus Google Scholar the of the pattern-recognition to or or to a of with the of and the lectin on the of or to of 6 pattern-recognition mannan-binding lectin or P. K. et through the lectin pathway of and PubMed Scopus Google Scholar pattern-recognition molecules with and activate and et of of PubMed Scopus Google Schwaeble W. et of the lectin pathway of complement in injury and 2021; 10: PubMed Scopus Google Scholar the and lectin and a to The of also in a A. et is a of kidney injury in Int. 2021; Full Text Full Text PDF PubMed Scopus Google to a lectin pathway has been shown to activate in the of or T. et pathway mannan-binding activate complement in of J. PubMed Scopus Google Scholar to complement with the pattern-recognition of the lectin pathway) also to A. R. et of complement and One. 2007; 2: PubMed Scopus Google Scholar evidence supporting the contribution of the alternative pathway to IgAN the of and in kidney F. Faria B. Schwaeble W. Daha M.R. 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