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A Novel Concept in the Pathogenesis of Collapsing Idiopathic Focal Segmental Glomerulosclerosis and HIV-Associated Nephropathy

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A Novel Concept in the Pathogenesis of Collapsing Idiopathic Focal Segmental Glomerulosclerosis and HIV-Associated Nephropathy J Am Soc Nephrol 10: 51–61, 1999 The Dysregulated Podocyte Phenotype: A Novel Concept in the Pathogenesis of Collapsing Idiopathic Focal Segmental Glomerulosclerosis and HIV-Associated Nephropathy LAURA BARISONI,* WILHELM KRIZ,† PETER MUNDEL,† and VIVETTE D’AGATI* *Department of Pathology, Columbia University College of Physicians and Surgeons, New York, New York; and †Department of Anatomy and Cell Biology, University of Heidelberg, Heidelberg, Germany. Abstract. Podocytes are highly differentiated, postmitotic cells, human kidney. In minimal change disease and membranous whose function is largely based on their complex cytoarchitec- glomerulopathy, all mature podocyte markers were retained at ture. The differentiation of podocytes coincides with progres- normal levels despite severe proteinuria and foot process fu- sive expression of maturity markers, including WT-1, CALLA, sion; no cell proliferation was observed. In contrast, in collaps- C3b receptor, GLEPP-1, podocalyxin, and synaptopodin. In ing idiopathic FSGS and HIV-associated nephropathy, there collapsing forms of focal segmental glomerulosclerosis was disappearance of all markers from all collapsed glomeruli (FSGS), including idiopathic FSGS and HIV-associated ne- and of synaptopodin from 16% of noncollapsed glomeruli. phropathy, podocytes undergo characteristic, irreversible ultra- This phenotypic dysregulation of podocytes was associated structural changes. This study analyzes the expression pattern with cell proliferation in both diseases. It is concluded that the of the above differentiation markers and of the proliferation loss of specific podocyte markers defines a novel dysregulated marker Ki-67 in collapsing idiopathic FSGS and HIV-associ- podocyte phenotype and suggests a common pathomechanism ated nephropathy compared with minimal change disease, in collapsing FSGS, whether idiopathic or HIV-associated. membranous glomerulopathy, as well as normal adult and fetal Podocytes are highly specialized cells whose functions include associated with a loss of proliferative activity and progressive support of the glomerular capillaries, synthesis of glomerular expression of distinctive podocyte markers, including the basement membrane, and regulation of glomerular permselec- Wilms’ tumor protein WT-1, CALLA (common acute lympho- tivity. These complex functions depend on a highly differen- blastic leukemia antigen), C3b receptor, GLEPP-1 (glomerular tiated and unique cytoarchitecture. Based on their cytoarchi- epithelial protein-1), podocalyxin, and synaptopodin. tecture, podocytes may be divided into three structurally and WT-1 is a critical protein in nephrogenesis, as indicated by functionally different segments: cell body, major processes, total failure of metanephric development in WT-1-deficient and foot processes. This segmentation of podocytes is also mice (4). Early in glomerular development, WT-1 is widely observed at the level of the cytoskeleton. Microtubules and expressed in glomerular progenitor cells, but becomes re- intermediate filaments predominate in cell bodies and major stricted to podocytes as the glomerulus matures. WT-1 is a zinc processes. The foot processes contain an actin-based contrac- finger transcription factor that downregulates proliferation (5), tile apparatus, which is linked to the GBM at focal contacts by but may also be necessary to maintain the mature podocyte a b an 3 1-integrin complex (reviewed in reference (1)). phenotype (6). The expression of these specialized cellular features is de- On their apical surface podocytes are equipped with a neg- velopmentally regulated. As the developing glomerulus passes atively charged glycocalyx which plays a dual role in perm- from the vesicle stage via the S-shaped body stage to the selectivity and maintenance of foot process cytoarchitecture. capillary loop stage and the mature glomerulus, podocytes Podocalyxin, the major sialoprotein of this glycocalyx, first acquire their characteristic complex cell architecture including appears in the S-shaped body stage of the developing glomer- foot processes and slit diaphragms (2,3). This maturation is ulus (7). In addition to podocytes, podocalyxin is also ex- pressed by endothelial cells (8). GLEPP-1, a podocyte-specific protein tyrosine phosphatase, is another integral apical mem- Received June 15, 1998. Accepted August 24, 1998. Parts of this work have been presented in abstract form at the 30th Annual brane protein that first appears in the S-shaped body stage. It Meeting of the American Society of Nephrology, San Antonio, Texas, No- has been proposed that signal transduction through GLEPP-1 is vember 2–5, 1997. involved in regulation of foot process dynamics, cell differen- Correspondence to Dr. Peter Mundel, Division of Nephrology, Albert Einstein tiation, and contact inhibition (9). College of Medicine, 1300 Morris Park Avenue, Bronx, NY 10461. Phone: 718-430-3158; Fax: 718-430-8963; E-mail: [email protected] A convergence has been demonstrated between antigenic determinants of B lymphocytes and leukemic cells on the one 1046-6673/1001-0051$03.00/0 Journal of the American Society of Nephrology hand and podocytes of fetal and adult kidney on the other. Copyright © 1999 by the American Society of Nephrology Acquisition or loss of these hematopoietic antigens has been 52 Journal of the American Society of Nephrology J Am Soc Nephrol 10: 51–61, 1999 correlated with the various stages of nephron differentiation Materials and Methods and development (10). Some of these antigens, such as CD35, We selected 28 cases from the archives of the Renal Pathology are expressed only transiently during the early stages of glo- Laboratory at Columbia Presbyterian Medical Center, including 10 merulogenesis, whereas others such as CALLA and C3b re- cases of collapsing idiopathic FSGS, eight cases of HIV-associated ceptor, whose expression first appears in the S-shaped body nephropathy, five cases of minimal change disease, and five cases of stage, are maintained in podocytes of the mature glomerulus membranous glomerulopathy. Normal fetal and adult kidney were (10,11). used as controls. Synaptopodin represents a novel proline-rich actin-associ- Three-micrometer-thick sections from each biopsy were stained with hematoxylin and eosin, periodic acid-Schiff, trichrome, and ated protein of telencephalic dendrites and glomerular podo- silver methenamine. Focal segmental and global glomerular sclerosis cytes that may play a role in the actin-based shape and motility as well as glomerular collapse were evaluated and expressed as of podocyte foot processes (12). During rat kidney develop- percentage of affected glomeruli per total number of glomeruli in each ment, synaptopodin first appears at the capillary loop stage. biopsy for each category. Sclerosis was defined as an expansile scar Thus, the expression of synaptopodin coincides with the for- of the glomerular tuft characterized by increased matrix, with or mation of foot processes (13). Because of its association with without associated hyalinosis and adhesion to Bowman’s capsule. a highly developed cytoskeletal architecture, synaptopodin is Collapse was defined as an implosive wrinkling and retraction of the an important marker of the mature podocyte phenotype. glomerular basement membrane, with resulting narrowing or obliter- In glomerular diseases with massive proteinuria, podocytes ation of capillary lumina and hypertrophy of overlying extracapillary undergo dramatic structural alterations. In some conditions, cells (16). such as minimal change disease, proteinuria and podocyte cellular alterations are reversible, whereas in other conditions, such as focal segmental glomerulosclerosis (FSGS), they are Immunohistochemistry not. Among the many forms of FSGS (14), the glomerular To characterize the expression profiles of podocyte marker proteins degeneration in collapsing idiopathic glomerulosclerosis and in glomerular development and in mature kidney, sections of normal HIV-associated nephropathy differs from that of other forms fetal and adult human kidney were studied by immunohistochemistry using the full panel of podocyte-specific antibodies (Table 1). In by its more severe clinical presentation, prognosis, and mor- addition, the proliferative activity of podocytes was analyzed using an phologic features. In these two diseases, the glomerular alter- antibody directed to the cell cycle protein Ki-67. Serial 3-mm-thick ations are characterized by segmental or global tuft collapse, sections of formalin-fixed paraffin-embedded tissue were obtained and most striking, the crowding of epithelial cells on the outer from the cases listed above. The sections were rehydrated in a graded aspect of the tuft. It also differs in its lack of synechiae, at least series of alcohol, blocked with 10% normal goat serum for polyclonal in the early stages. It has been suggested that a primary antibodies in 1% bovine serum albumin and 10% normal horse serum podocyte injury plays a central role in the pathogenesis of for monoclonal antibodies in 1% bovine serum albumin, and stained certain forms of FSGS (15), although the nature of this inju- using avidin-biotin immunoperoxidase technique with monoclonal rious factor remains to be discovered. antibodies against GLEPP-1 (reference 9; courtesy of R.C. Wiggins, The current study was designed to investigate to what extent Ann Arbor, MI), podocalyxin (courtesy of R.C. Wiggins), synaptopo- the morphologic alterations seen in collapsing idiopathic glo- din (12,13), and Ki-67
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