Clinical, morphologic, and genetic features of renal leukocyte chemotactic factor 2 amyloidosis
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1 & 2014 International Society of Nephrology see commentary on page 229 Clinical, morphologic, and genetic features of renal leukocyte chemotactic factor 2 amyloidosis Christopher P. Larsen 1, Robert J. Kossmann 2, Marjorie L. Beggs 1, Alan Solomon 3 and Patrick D. Walker 1 1 Nephropath, Little Rock, Arkansas, USA; 2 Human Immunology and Cancer Program, University of Tennessee Graduate School of Medicine, Knoxville, Tennessee, USA and 3 Nephrophiles, Santa Fe, New Mexico, USA Leukocyte chemotactic factor 2 amyloidosis (ALECT2) is a recently described form of amyloidosis that most frequently manifests clinically with progressive renal failure. In a series of 414 cases of amyloidosis, there were 40 cases of ALECT2: the second most common type of renal amyloidosis in this series. This was particularly common in Hispanic patients in the Southwest United States, where more than half of amyloidosis cases were ALECT2. It is possible that this represents a familial amyloidosis as there were two brothers with ALECT2 in our study. Morphologically, there was consistent amyloid deposition in the renal cortex with medullary involvement in only about a third of cases. There were no mutations detected in the LECT2 gene, although all patients tested were homozygous for the G nucleotide in a non-synonymous SNP at position 172. Most patients presented with chronic kidney disease and, on follow-up, showed progression with an average deterioration in renal function of 0.5 ml/min/1.73 m 2 per month. Unfortunately, the etiology of ALECT2 is currently unknown and there is currently no efficacious treatment of the disease. Kidney International (2014) 86, ; doi: /ki ; published online 12 February 2014 Amyloidosis is the abnormal deposition and accumulation of insoluble protein fibrils in organs or tissues. These proteins deposit with a characteristic beta-pleated sheet conformation, which leads to the diagnostic morphologic finding of Congo red-positive staining with green birefringence upon polarization. The kidney is the most common organ involved in systemic amyloidosis, commonly leading to renal failure and the nephrotic syndrome. 1 There are now 30 proteins known to form amyloid in humans. 2 The most prevalent type in the United States, designated as AL, is derived from immunoglobulin light chains, although many other kinds of amyloid deposit in the kidney, including those formed from serum amyloid A protein (AA), and, less commonly, fibrinogen (AFib), transthyretin (ATTR), lysozyme (ALys), and apolipoproteins AI or AII (AApoAI, AApoAII). One of the most recently described forms of amyloidosis is derived from leukocyte chemotactic factor 2 (ALECT2). It exhibits a morphologic pattern with extensive congophilic deposits present in the glomeruli, interstitium, and vessels in previous series. 3,4 Patients with ALECT2 typically present with progressive renal failure secondary to the deposition of insoluble protein aggregates. 5 We present the largest renal biopsy series to date and detail the clinical, morphologic, and genetic features of ALECT2. Correspondence: Christopher P. Larsen, Nephropath, Executive Center Drive, Suite 100, Little Rock, Arkansas 72211, USA. chris.larsen@nephropath.com Received 9 September 2013; revised 16 December 2013; accepted 19 December 2013; published online 12 February 2014 RESULTS Among the 23,650 adult native kidney biopsy specimens processed at Nephropath since 2009, 40 (0.2%) cases of LECT2 amyloidosis were found among 414 total cases of amyloidosis. As can be seen in Table 1, there was a distinct geographic and ethnic preponderance to these cases. Hispanics comprise B10% of the patients in our renal biopsy practice, yet 35/40 (88%) of the patients with ALECT2 are Hispanic. The remaining patients included three Native American Indians from the Southwest United States, one Caucasian, and one native Israeli. Two of the patients in this series are siblings. There was a particularly high density of ALECT2 from the Southwestern United States, including New Mexico, Arizona, and far west Texas (high desert region), where 2% of total biopsies during the time period of this study were diagnosed as ALECT2 and 54% of amyloidosis cases from this area were ALECT2 (Table 1). 378 Kidney International (2014) 86,
2 CP Larsen et al.: Renal LECT2 amyloidosis Table 1 Frequency of amyloid type Southwest US Remainder of US Total Total biopsies received ,562 22,606 Total biopsies showing ALect2, n (%) 21 (2%) 19 (0.1%) 40 (0.2%) Total amyloid cases 39 (3.7%) 375 (1.7%) 414 (1.8%) AL/AH, n (% of amyloid cases) 16 (41%) 329 (88%) 345 (83.3%) ALect2, n (% of amyloid cases) 21 (54%) 19 (5%) 40 (10%) AA, n (% of amyloid cases) 2 (5%) 19 (5%) 21 (5%) Afib, n (% of amyloid cases) 0 (0%) 4 (1%) 4 (1%) AApoAIV, n (% of amyloid cases) 0 (0%) 2 (1%) 2 (1%) Unknown, n (% of amyloid cases) 0 (0%) 2 (1%) 2 (1%) Table 2 Clinical finding in patients with LECT2 amyloidosis Clinical findings Mean age at biopsy (years) 70.6 Gender (male/female) 25/15 Ethnicity Hispanic 88% Native American 8% Caucasian 3% Native Israeli 3% Mean serum Cr at time of biopsy (n ¼ 40) 2.8 mg/dl Mean 24 h proteinuria at time of biopsy (n ¼ 40) 2.1 g/24 h Patients with normal urine protein at time of biopsy 16/40 (40%) Indication for biopsy Chronic kidney disease 24/40 (60%) Acute on chronic kidney disease 3/40 (8%) Proteinuria 13/40 (33%) Past medical history Diabetes mellitus 15/40 (38%) Hypertension 20/40 (50%) Monoclonal gammopathy of undetermined significance 3/40 (8%) Follow-up Stable renal function 2/21 (10%) Progressive renal failure 13/21 (62%) End-stage kidney disease 6/21 (29%) Most patients were elderly, with a mean age at diagnosis of 70.4 years (range years). Chronic kidney disease was the primary indication for biopsy in 24/40 patients. Many of the patients did not have proteinuria, with 16/40 cases (40%) having o200 mg/day. There were nine patients with nephrotic range proteinuria, but eight of these nine had a second glomerulopathy present on biopsy that likely contributed to the degree of proteinuria (Table 2). The exonic regions of the LECT2 gene were sequenced in 10 patients (including the siblings with disease) and the entire gene including exons, introns, and the promoter region was sequenced in three patients. All 10 patients were homozygous for the G nucleotide in a non-synonymous SNP at position 172 (SNP rs31517). This is a common polymorphism with a G allele frequency of 0.51 in samples Table 3 Morphology of LECT2 amyloidosis Findings on renal biopsy % Of cases with deposition Location of amyloid deposition in this location Glomerular 88 Interlobular-size artery or larger 57 Arteriole 83 Cortex interstitium 100 Medulla interstitium 33 % Of cases with specified Concurrent glomerulonephritis present glomerulonephritis Nodular diabetic glomerulosclerosis 21 Membranous glomerulopathy 5 ANCA-associated crescentic glomerulonephritis 3 Focal segmental glomerulosclerosis 3 from patients of Mexican ancestry. No mutations were detected in any of these patients. Follow-up data were available in 21 patients and are detailed in Table 2. Most of the patients had some degree of chronic kidney disease on presentation. Two of the patients were found to have end-stage kidney disease on presentation and proceeded immediately to dialysis. Four additional patients proceeded to dialysis over a mean of 120 months. Nineteen patients were followed for a mean of 49.6 months (range months) and showed a mean drop in egfr of 0.5 ml/min/1.73 m 2 per month. All cases showed deposition of amyloidosis in the renal cortex (Table 3 and Figure 1). Glomerular and arteriolar deposition was almost as common as involvement of the cortical interstitium. Amyloid deposition in the interlobular and arcuate arteries is considerably less common as was interstitial deposition in the renal medulla. When present, medullary interstitial deposition was sparse and considerably less prominent than that seen in the cortical interstitium. Immunohistochemical studies showed strong staining for antibodies directed against LECT2 within the amorphous material in all patients, whereas stains for AA, lambda, kappa, fibrinogen, and immunoglobulins were negative (Figure 2). Ultrastructural examination showed evidence of small, nonbranching, overlapping fibrils within the cortical interstitium of all patients and within the mesangium of patients with glomerular involvement. Two patients had a tissue diagnosis on previous biopsies, including one with known amyloidosis on a previous prostate biopsy and the second with a diagnosis of amyloidosis on a liver biopsy. DISCUSSION We present the largest case series of ALECT2 to date and describe the first report of familial involvement. This case series confirms previous findings, which state that in the United States ALECT2 is one of the most common forms of renal amyloidosis. 6 Further, we have shown that in the Southwestern United States the incidence is much higher as it is the most common form of amyloidosis in this region. Kidney International (2014) 86,
3 CP Larsen et al.: Renal LECT2 amyloidosis Cortex Medulla Figure 1 Leukocyte chemotactic factor 2 amyloidosis. (a) Extensive Congo red-positive amyloid deposition is present in the cortex, which abruptly stops at the corticomedullary junction with no deposition in the medulla (original magnification 20). (b) Higher power view of cortex revealing amyloid deposition throughout the interstitium and in glomeruli (Congo red stain; original magnification 100). (c) There is no medullary involvement by the amyloid deposition (Congo red stain; original magnification 100). Figure 2 Leukocyte chemotactic factor 2 amyloidosis. (a) Transmission electron photomicrograph of the interstitial region shows deposits of randomly arranged fibrils (unstained; original magnification 30,000). (b) Glomerular and interstitial amyloid deposits show reactivity with an anti-lect2 antibody (immunoperoxidase technique, original magnification 200). The strong ethnic preponderance and evidence of familial involvement are suggestive of a genetic etiology to this disease. The clinical presentation is frequently atypical for amyloidosis as many cases do not show significant proteinuria unless a second concurrent glomerulopathy is present. Despite being one of the last known amyloid proteins described, ALECT2 is actually quite prevalent. Two previous large case series focusing on renal amyloidosis found ALECT2 to be the third most common form of amyloidosis involving the kidney, closely following AA amyloid.4,6 In addition, a large case series detailing amyloidosis in the liver identified it as the second most common form of hepatic amyloidosis.7 We show in this, the largest case series of ALECT2 to date, that it is the second most common form of amyloidosis as a whole and is particularly common in Hispanic patients from the Southwest United States. Given the regional variation in LECT2 amyloidosis shown in this 380 study, the overall prevalence of ALECT2 in a given practice will vary depending upon the geographic location and ethnic makeup of the patient population. Other case series and case reports have shown that there are likely other ethnic groups with unique susceptibility to ALECT2, including Sudanese8 and Punjabi people.9 There are consistent features to the morphologic pattern of amyloid deposition in ALECT2. There is always interstitial deposition within the cortex. Most cases will also show glomerular and arteriolar involvement, although these can be quite mild. The medulla is not involved by amyloid deposition in most cases. This stands in contrast to other forms of amyloidosis with distinctive morphologic patterns such as AApoAIV, with predominantly medullary involvement,10 and Afib, which typically shows florid deposition restricted to the glomeruli.1 We have also noted that the amyloid of ALECT2 is strikingly congophilic. Kidney International (2014) 86,
4 CP Larsen et al.: Renal LECT2 amyloidosis ALECT2 is unique among amyloidoses in that the underlying etiology is currently unknown. The majority of familial amyloidoses result from the production of an aberrant protein with increased amyloidogenic potential. This is not the case in ALECT2. Sequencing of 26 patients has failed to uncover a single case with mutations in the LECT2 gene itself (16 cases previously reported in addition to the 10 in this series). 3,5,9 Although no causative mutations have been described in this disease, all 26 patients with sequencing of the LECT2 gene are homozygous for the G nucleotide in a non-synonymous SNP at position 172 (SNP rs31517). This is a common polymorphism with a G allele frequency of 0.51 in samples from patients of Mexican ancestry. The overrepresentation of this common polymorphism in patients with ALECT2 indicates that it is necessary but not sufficient to cause disease. It has been hypothesized that this polymorphism increases the amyloidogenic propensity of this protein variant. 5 However, it is also possible that this polymorphism segregates with some other, as yet unknown, causative mutation and does not actually have any role in the disease. Two patients with ALECT2 were tested for serum LECT2 concentrations and neither showed elevated values, suggesting that systemic overexpression of the LECT2 protein is not the etiology. 5 Thus, the underlying etiology of ALECT2 remains a mystery at this time. The prognosis for patients with ALECT2 is guarded. Most of the patients in this series had significant chronic kidney disease at the time of presentation and the disease was progressive in most with a mean fall in egfr of 0.5 ml/min/ 1.73 m 2 per month. Nevertheless, the mean age at biopsy was over the age of 70 years and the youngest patient identified with disease was 52 years old. Therefore, most patients will maintain renal function until late in life. It is not known whether ALECT2 deposition is a slow process that begins early in life remaining undetected until significant accumulation has occurred, or whether the deposition of the aberrant protein is a more rapid process that begins later in life. There is no specific treatment for ALECT2, although it is important to accurately diagnose this type of amyloid to avoid mistreatment of ALECT2 as though it were AL amyloidosis. ALECT2 is an emerging disease that is beginning to be recognized as an important cause of end-stage renal disease in patients of Hispanic ethnicity. There are several factors that suggest ALECT2 is a familial amyloidosis, including the strong Hispanic preponderance and known familial involvement. In addition, the pathogenesis of all familial amyloidoses described thus far are Mendelian disorders. 11 It is our hypothesis that ALECT2 is a digenic disease in which the combination of the common LECT2 G/G genotype at position 172 and some other, as yet uncharacterized, mutation results in disease. Further studies are currently underway to test this hypothesis. METHODS Renal biopsies were processed using methods that are in routine use in our lab and as described in our previous reports. 12 All data were collected according to protocols approved by Schulman Institutional Review Board. Light microscopy Briefly, kidney biopsies were fixed in buffered formalin, dehydrated in graded alcohols, and embedded in paraffin using standard techniques. Serial 3-mm-thick sections were cut and treated with hematoxylin and eosin, Jones methenamine silver, Masson trichrome, and periodic acid-schiff reagent. In addition, the tissue was stained with Congo red in which the diagnosis of amyloid was confirmed by Congo red positivity with apple-green birefringence when viewed by polarizing microscopy. Immunohistochemistry Samples were placed in Michel s media, washed in buffer, and frozen in a cryostat. Sections, cut at 5 mm, were rinsed in buffer and reacted with fluorescein-tagged polyclonal rabbit anti-human antibodies to IgG, IgA, IgM, C3, C4, C1q, fibrinogen, and k, and l light chains (Dako, Carpenteria, CA) for 1 h, rinsed, and a coverslip applied using aqueous mounting media. Immunohistochemical analysis for AA and LECT2 amyloid was performed in all cases. Paraffinembedded sections of 4-mm thickness were cut, deparaffinized, rehydrated, and blocked with normal horse serum for 5 min, followed by a reaction for 1 h with a 1:200 dilution of mouse antihuman amyloid A protein mab (Dako, Carpenteria, CA) or with a 1:40 dilution of a mouse anti-human LECT2 mab (R&D Systems, Minneapolis, MN). Electron microscopy Samples of 1-mm thickness were removed from each end of the renal biopsy specimen and dehydrated using graded series of alcohols, followed by embedding in epon/araldite embedding resin. Sections of 1-mm thickness were cut with an ultramicrotome stained with toluidine blue to identify areas containing amyloid. Thin sections were then cut with an ultramicrotome and examined in a Jeol JEM-1011 electron microscope. Photomicrographs were routinely taken at 5000, 12,000, and 20,000. To confirm the fibrillar nature of the deposits, appropriate areas were examined at 50,000. Sequencing DNA was extracted from blood using the PreAnalytiX kit (Qiagen, Valencia, CA). Primers were designed using DNAstar PrimerSelect to encompass the entire gene in fragment of B bp using Phusion High-Fidelity PCR master mix with HF buffer (Thermo- Scientific, Waltham, MA). The PCR products were purified using Qiagen PCR purification columns. The product was checked for size using the Agilent DNA 1000 kit (Agilent, Santa Clara, CA) and was Sanger sequenced. The data were aligned using the SeqMan Pro program (DNAstar, Madison, WI) and blasted to the NCBI database. DISCLOSURE All the authors declared no competing interests. REFERENCES 1. von Hutten H, Mihatsch M, Lobeck H et al. Prevalence and origin of amyloid in kidney biopsies. Am J Surg Pathol 2009; 33: Kidney International (2014) 86,
5 CP Larsen et al.: Renal LECT2 amyloidosis 2. Sipe JD, Benson MD, Buxbaum JN et al. Amyloid fibril protein nomenclature: 2012 recommendations from the Nomenclature Committee of the International Society of Amyloidosis. Amyloid 2012; 19: Benson MD, James S, Scott K et al. Leukocyte chemotactic factor 2: a novel renal amyloid protein. Kidney Int 2008; 74: Larsen CP, Walker PD, Weiss DT et al. Prevalence and morphology of leukocyte chemotactic factor 2-associated amyloid in renal biopsies. Kidney Int 2010; 77: Murphy CL, Wang S, Kestler D et al. Leukocyte chemotactic factor 2 (LECT2)-associated renal amyloidosis: a case series. Am J Kidney Dis 2010; 56: Said SM, Sethi S, Valeri AM et al. Renal amyloidosis: origin and clinicopathologic correlations of 474 recent cases. Clin J Am Soc Nephrol 2013; 8: Vrana JA, Theis JD, Wu TT et al. Amyloidosis of the liver: mass spectrometry-based analysis reveals diverse etiology associated with distinct histological features. Modern Pathol 2012; S25: Holanda DG, Acharya VK, Dogan A et al. Atypical presentation of atypical amyloid. Nephrol Dial Transplant 2011; 26: Dogan A, Theis JD, Vrana JA. Clinical and pathological phenotype of leukocyte cell-derived chemotaxin-2 (LECT2) amyloidosis (ALECT2). Amyloid 2010; 17: Sethi S, Theis JD, Shiller SM et al. Medullary amyloidosis associated with apolipoprotein A-IV deposition. Kidney Int 2012; 81: Jennette JC, Olson JL, Schwartz MM et al. (eds) Heptinstall s Pathology of the Kidney, 6th edn Lippincott Williams & Wilkins: Philadelphia, Walker PD, Cavallo T, Bonsib SM. Practice guidelines for the renal biopsy. Mod Pathol 2004; 17: Kidney International (2014) 86,
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