Gangliosides in Podocyte Biology and Disease

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2020 Dec 22

PMID 33348903

Citations 10

Authors

Berkan Savas

Giuseppe Astarita

Massimo Aureli

Dil Sahali

Mario Ollero

Affiliations

Soon will be listed here.

Abstract

Gangliosides constitute a subgroup of glycosphingolipids characterized by the presence of sialic acid residues in their structure. As constituents of cellular membranes, in particular of raft microdomains, they exert multiple functions, some of them capital in cell homeostasis. Their presence in cells is tightly regulated by a balanced expression and function of the enzymes responsible for their biosynthesis, ganglioside synthases, and their degradation, glycosidases. The dysregulation of their abundance results in rare and common diseases. In this review, we make a point on the relevance of gangliosides and some of their metabolic precursors, such as ceramides, in the function of podocytes, the main cellular component of the glomerular filtration barrier, as well as their implications in podocytopathies. The results presented in this review suggest the pertinence of clinical lipidomic studies targeting these metabolites.

Citing Articles

The good, the bad, and the unknown nature of decreased GD3 synthase expression.

Puljko B, Grbavac J, Potocki V, Ilic K, Viljetic B, Kalanj-Bognar S Front Mol Neurosci. 2024; 17:1465013.

PMID: 39649107 PMC: 11621222. DOI: 10.3389/fnmol.2024.1465013.

Mechanistic and Therapeutic Implications of Protein and Lipid Sialylation in Human Diseases.

Zhong X, DAntona A, Rouse J Int J Mol Sci. 2024; 25(22).

PMID: 39596031 PMC: 11594235. DOI: 10.3390/ijms252211962.

Sphingolipids and Chronic Kidney Disease.

Sakic Z, Atic A, Potocki S, Basic-Jukic N J Clin Med. 2024; 13(17).

PMID: 39274263 PMC: 11396415. DOI: 10.3390/jcm13175050.

Hematopoietic stem cell transplantation leads to biochemical and functional correction in two mouse models of acid ceramidase deficiency.

Rybova J, Sundararajan T, Kuchar L, Dlugi T, Ruzicka P, McKillop W Mol Ther. 2024; 32(10):3402-3421.

PMID: 39108096 PMC: 11489543. DOI: 10.1016/j.ymthe.2024.08.004.

Lipidomic Profiling of Kidney Cortical Tubule Segments Identifies Lipotypes with Physiological Implications.

Cheval L, Poindessous V, Sampaio J, Crambert G, Pallet N Function (Oxf). 2024; 5(4).

PMID: 38985001 PMC: 11237892. DOI: 10.1093/function/zqae016.

References

Yamashita T, Hashiramoto A, Haluzik M, Mizukami H, Beck S, Norton A . Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc Natl Acad Sci U S A. 2003; 100(6):3445-9. PMC: 152312. DOI: 10.1073/pnas.0635898100. View

Grimbert P, Valanciute A, Audard V, Pawlak A, Le gouvelo S, Lang P . Truncation of C-mip (Tc-mip), a new proximal signaling protein, induces c-maf Th2 transcription factor and cytoskeleton reorganization. J Exp Med. 2003; 198(5):797-807. PMC: 1865475. DOI: 10.1084/jem.20030566. View

Kwak D, Rho Y, Kwon O, Ahan S, Song J, Choo Y . Decreases of ganglioside GM3 in streptozotocin-induced diabetic glomeruli of rats. Life Sci. 2003; 72(17):1997-2006. DOI: 10.1016/s0024-3205(03)00090-0. View

Aguilar R, Genta S, Sanchez S . Renal gangliosides are involved in lead intoxication. J Appl Toxicol. 2007; 28(2):122-31. DOI: 10.1002/jat.1256. View

Mauri L, Sonnino S, Prinetti A . Chemical and Physicochemical Properties of Gangliosides. Methods Mol Biol. 2018; 1804:1-17. DOI: 10.1007/978-1-4939-8552-4_1. View

Simons M, Schwarz K, Kriz W, Miettinen A, Reiser J, Mundel P . Involvement of lipid rafts in nephrin phosphorylation and organization of the glomerular slit diaphragm. Am J Pathol. 2001; 159(3):1069-77. PMC: 1850447. DOI: 10.1016/S0002-9440(10)61782-8. View

Yoo T, Pedigo C, Guzman J, Correa-Medina M, Wei C, Villarreal R . Sphingomyelinase-like phosphodiesterase 3b expression levels determine podocyte injury phenotypes in glomerular disease. J Am Soc Nephrol. 2014; 26(1):133-47. PMC: 4279736. DOI: 10.1681/ASN.2013111213. View

Simons K, Gerl M . Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010; 11(10):688-99. DOI: 10.1038/nrm2977. View

Yoon S, Nakayama K, Hikita T, Handa K, Hakomori S . Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc Natl Acad Sci U S A. 2006; 103(50):18987-91. PMC: 1748164. DOI: 10.1073/pnas.0609281103. View

10.

Zhang T, de Waard A, Wuhrer M, Spaapen R . The Role of Glycosphingolipids in Immune Cell Functions. Front Immunol. 2019; 10:90. PMC: 6361815. DOI: 10.3389/fimmu.2019.00090. View

11.

Jackson S, Colsch B, Egan T, Lewis E, Schultz J, Woods A . Gangliosides' analysis by MALDI-ion mobility MS. Analyst. 2010; 136(3):463-6. PMC: 7543062. DOI: 10.1039/c0an00732c. View

12.

Oniszczuk J, Sendeyo K, Chhuon C, Savas B, Cogne E, Vachin P . CMIP is a negative regulator of T cell signaling. Cell Mol Immunol. 2019; 17(10):1026-1041. PMC: 7609264. DOI: 10.1038/s41423-019-0266-5. View

13.

Matsuura M, Kikkawa Y, Akashi K, Kitagawa T, Inage Z, Iwamori M . Thyroid antigen-antibody nephritis: possible involvement of fucosyl-GM1 as the antigen. Endocrinol Jpn. 1987; 34(4):587-93. DOI: 10.1507/endocrj1954.34.587. View

14.

Kabayama K, Sato T, Saito K, Loberto N, Prinetti A, Sonnino S . Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc Natl Acad Sci U S A. 2007; 104(34):13678-83. PMC: 1949342. DOI: 10.1073/pnas.0703650104. View

15.

Glebov O, Nichols B . Lipid raft proteins have a random distribution during localized activation of the T-cell receptor. Nat Cell Biol. 2004; 6(3):238-43. DOI: 10.1038/ncb1103. View

16.

Galeazzi M, Annunziata P, Sebastiani G, Bellisai F, Campanella V, Ferrara G . Anti-ganglioside antibodies in a large cohort of European patients with systemic lupus erythematosus: clinical, serological, and HLA class II gene associations. European Concerted Action on the Immunogenetics of SLE. J Rheumatol. 2000; 27(1):135-41. View

17.

Iwabuchi K . Gangliosides in the Immune System: Role of Glycosphingolipids and Glycosphingolipid-Enriched Lipid Rafts in Immunological Functions. Methods Mol Biol. 2018; 1804:83-95. DOI: 10.1007/978-1-4939-8552-4_4. View

18.

Janecke A, Xu R, Steichen-Gersdorf E, Waldegger S, Entenmann A, Giner T . Deficiency of the sphingosine-1-phosphate lyase SGPL1 is associated with congenital nephrotic syndrome and congenital adrenal calcifications. Hum Mutat. 2017; 38(4):365-372. PMC: 5384969. DOI: 10.1002/humu.23192. View

19.

Merscher S, Fornoni A . Podocyte pathology and nephropathy - sphingolipids in glomerular diseases. Front Endocrinol (Lausanne). 2014; 5:127. PMC: 4115628. DOI: 10.3389/fendo.2014.00127. View

20.

Schumann J, Grevot A, Ledieu D, Wolf A, Schubart A, Piaia A . Reduced Activity of Sphingosine-1-Phosphate Lyase Induces Podocyte-related Glomerular Proteinuria, Skin Irritation, and Platelet Activation. Toxicol Pathol. 2015; 43(5):694-703. DOI: 10.1177/0192623314565650. View