Nonimmune binding of human immunoglobulins G and A by Streptococcus pyogenes: the role of this phenomenon in pathology

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Abstract

M and M-like proteins are key pathogenicity factors of Streptococcus pyogenes, a widely prevalent and potentially lethal bacterium. These proteins confer resistance to the host’s innate and adaptive immune response by attracting specific human proteins to the streptococcal surface. The nonimmune binding of host immunoglobulins G (IgG) and A (IgA) to M and M-like proteins via their Fc domains was first described over 50 years ago, but its role in the pathogenicity of S. pyogenes remains unclear. This discovery has had a significant impact on the development of innovative diagnostic approaches, technologies, and tools in microbiology, immunology, and molecular biology. The nonimmune binding of immunoglobulins has been suggested to play a role in immune conditions on mucosal surfaces and their secretions, but not in blood plasma, while other studies suggest it protects microbes from phagocytosis in the host’s nonimmune blood. The Fc-binding effect has been shown to increase the pathogenicity of streptococci, contributing to the development of autoimmune diseases and tissue damage in experimental animals. The experimental autoimmune process can be prevented by administering purified Fc fragments of immunoglobulins to animals. Streptococcal diseases play a significant role in the pathogenesis of IgA-nephropathy (IgAN), a mesangial proliferative process caused by initial IgA-Fcα deposition in renal mesangium cells. Literature suggests a relevance of recent ideas about the important role of nonimmune Ig binding in streptococcal diseases, and further efforts are required to study the binding of Fc fragments of IgG and IgA to M and M-like proteins of S. pyogenes, with the aim of developing preventive and potentially therapeutic applications. The paper speculates on the role of nonimmune Ig binding in streptococcal diseases, including cases with various mechanisms of development. These studies also focuses on preventive and potentially therapeutic applications of Fc fragments of IgG to M or M-like proteins of S. pyogenes.

About the authors

Larisa A. Burova

Institute of Experimental Medicine

Author for correspondence.
Email: lburova@yandex.ru
ORCID iD: 0000-0001-7687-2348
SPIN-code: 6084-1255
Scopus Author ID: 7003982261
ResearcherId: E-5270-2014

MD, Dr. Sci. (Med.), Leading Research Associate, Department of Molecular Microbiology

Russian Federation, Saint Petersburg

Alexander N. Suvorov

Institute of Experimental Medicine; Saint Petersburg State University

Email: alexander_suvorov1@hotmail.com
ORCID iD: 0000-0003-2312-5589
SPIN-code: 8062-5281
Scopus Author ID: 7101829979
ResearcherId: J-6921-2013

MD, Dr. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences, Head Department of Molecular Microbiology; Head Department of Fundamental Medicine and Medical Technologies

Russian Federation, Saint Petersburg; Saint Petersburg

Peter V. Pigarevsky

Institute of Experimental Medicine

Email: pigarevsky@mail.ru
ORCID iD: 0000-0002-5906-6771
SPIN-code: 8636-4271
Scopus Author ID: 55404484800
ResearcherId: C-3425-2014

Dr. Sci. (Biol.), Head Department of General Morphology

Russian Federation, Saint Petersburg

Artem A. Totolian

Institute of Experimental Medicine

Email: totolyan@hotmail.com
ORCID iD: 0000-0002-3310-9294
SPIN-code: 1741-9171
Scopus Author ID: 7004990713
ResearcherId: J-4218-2014

MD, Dr. Sci. (Med.), Professor, Academician RAS, Chief Research Associate, Department of Molecular Microbiology

Russian Federation, Saint Petersburg

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2. Fig. 1. Immunomorphological changes in cortical and medullary layers of the rabbit kidney, induced by Streptococcus pyogenes strain emm12 [43]: a — the expression of TNF-α by glomeruli mesangial cells (arrow); b — IgG deposition in the wall of the proximal tubule (arrow); c — deposition of C3 component of complement in the cells of the distal tubules (arrows); d — atrophy of the tissues of the renal glomeruli, the abundance of red blood cells in the cavity. a–c — immunohistochemical staining, ×750; d — staining with hematoxylin-eosin, ×550

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3. Fig. 2. Membranous-proliferative glomerulonephritis in a rabbit after injection of IgGFc-positive GAS strain of type M1 [81]: a — thickening of the basement membrane and interposition of mesangium cells, ×8000; b — fusion of podocyte and membrane, disintegration of endothelium, ×8500; c — interposition of mesangium and degranulation of basophils in capillaries, ×8000; d — hypertrophy and disintegration of podocytes, endothelium, fragments of cells in vessels, ×13500

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4. Fig. 3. Morphological changes in cortex and medullar substances of the rabbit renal tissue induced by Streptococcus pyogenes of genotype emm1 [82]: a — the capsular cavities of the glomeruli strongly expanded, in the capillary loops of the glomeruli necrosis and atrophy are observed, in the wall of the proximal tubules of the cortex desquamation of epithelial cells is revealed (shown by arrows); b — swelling and thickening of the membranes of the wall of distal tubules in the medulla with the simultaneous proliferation of the fibrous interstitial tissue; c, d — absence of pathological changes in the cortex and the medulla of the kidney obtained from rabbits treated with Fc fragments of IgG. Staining with hematoxylin-eosin, ×750

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5. Fig. 4. Histological changes detected in rabbit kidney after injection of a recombinant Fcγ-protein from the GAS strain genotype emm12 (our new unpublished data): a — pathologically altered glomeruli are visible in the cortical layer, capsule cavities are expanded or compressed, necrosis and atrophy in capillary loops, destruction is observed in the proximal tubules; b — the wall of the tubules is thickened and edematous or atrophic. Epithelial cells of the lumen of the tubules with signs of necrosis; protein masses are detected; c — lymphocytic infiltrates are detected; they are dominated by small and medium lymphocytes, immature and mature plasma cells. a, b — staining with hematoxylin-eosin, a — ×250, b — ×500; c — immunohistochemical staining, ×750

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6. Fig. 5. Morphological changes (shown by arrows) in the myocardium of the rabbit after injection of Streptococcus pyogenes type M1, binding the Fc fragment of human or rabbit IgG [45]: a–c — the destruction of mitochondria and myofibrils (ТЕМ ×16000, 16000 and 24000, respectively); d — the morphology of the normal rabbit myocardium, which received injection of control IgG Fc-negative strain (ТЕМ ×16000)

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7. Fig. 6. Immunomorphological changes in the cortical and medullary substances of the rabbit kidney induced by Streptococcus pyogenes type M60 [105]: a, b — deposits of IgA in the mesangial cells of the renal glomeruli (arrows); c — deposition of C3-complement components in the cells of the tubules (arrows) of the medullary layer of the kidney; d — deposits of C3 component complement in the cells of the proximal tubules (arrows) surrounding the renal glomerulus in the cortical substance. Immunohistochemical staining, ×750

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