Home LiteratureArticle Details
PMID: 19164451 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Alternative splicing of the murine receptor for advanced glycation end-products (RAGE) gene.

Kalea AZ, Reiniger N, Yang H, Arriero M, Schmidt AM, Hudson BI

Abstract

The alternative splicing of pre-mRNAs is a critical mechanism in genomic complexity, disease, and development. Studies of the receptor for advanced glycation end-products (RAGE) indicate that this gene undergoes a variety of splice events in humans. However, no studies have extensively analyzed the tissue distribution in other species or compared evolutionary differences of RAGE isoforms. Because the majority of studies probing RAGE function have been performed in murine models, we therefore performed studies to identify and characterize the splice variants of the murine RAGE gene, and we compared these to human isoforms. Here, using mouse tissues, we identified numerous splice variants including changes in the extracellular domain or the removal of the transmembrane and cytoplasmic domains, which produce soluble splice isoforms. Comparison of splice variants between humans and mice revealed homologous regions in the RAGE gene that undergo splicing as well as key species-specific mechanisms of splicing. Further analysis of tissue splice variant distribution in mice revealed major differences between lung, kidney, heart, and brain. To probe the potential impact of disease-like pathological states, we studied diabetic mice and report that RAGE splice variation changed dramatically, resulting in an increase in production of soluble RAGE (sRAGE) splice variants, which were not associated with detectable levels of sRAGE in murine plasma. In conclusion, we have determined that the murine RAGE gene undergoes extensive splicing with distinct splice isoforms being uniquely distributed in different tissues. These differences in RAGE splicing in both physiological and pathogenic states further expand our understanding of the biological repertoire of this receptor in health and disease.

MeSH Terms
Alternative Splicing Animals Base Sequence Computational Biology Female Glycation End Products, Advanced Humans Male Mice Molecular Sequence Data Protein Isoforms/genetics,metabolism Receptor for Advanced Glycation End Products Receptors, Immunologic/genetics,metabolism Sequence Homology, Nucleic Acid Tissue Distribution
Chemicals
Glycation End Products, Advanced Protein Isoforms Receptor for Advanced Glycation End Products Receptors, Immunologic
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kalea Anastasia Z
Division of Surgical Science, Dept. of Surgery, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA.
Reiniger Nina
Yang Hojin
Arriero Maria
Schmidt Ann Marie
Hudson Barry I
References (41)
41 references, click to expand
  1. Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-kappaB require the cytoplasmic domain of the receptor but different downstream signaling pathways.
    J Biol Chem. 1999 Jul 9;274(28):19919-24 PMID: 10391939
  2. Identification, classification, and expression of RAGE gene splice variants.
    FASEB J. 2008 May;22(5):1572-80 PMID: 18089847
  3. Low conservation of alternative splicing patterns in the human and mouse genomes.
    Hum Mol Genet. 2003 Jun 1;12(11):1313-20 PMID: 12761046
  4. Identification of mouse orthologue of endogenous secretory receptor for advanced glycation end-products: structure, function and expression.
    Biochem J. 2006 May 15;396(1):109-15 PMID: 16503878
  5. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins.
    J Biol Chem. 1992 Jul 25;267(21):14998-5004 PMID: 1378843
  6. Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice.
    J Clin Invest. 2008 Jan;118(1):183-94 PMID: 18079965
  7. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system.
    J Biol Chem. 1995 Oct 27;270(43):25752-61 PMID: 7592757
  8. Expression of a novel secreted splice variant of the receptor for advanced glycation end products (RAGE) in human brain astrocytes and peripheral blood mononuclear cells.
    Mol Immunol. 2004 Mar;40(16):1203-11 PMID: 15104125
  9. Circulating levels of soluble receptor for advanced glycation end products in Alzheimer disease and vascular dementia.
    Arch Neurol. 2005 Nov;62(11):1734-6 PMID: 16286548
  10. Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE).
    J Biol Chem. 2004 Nov 26;279(48):50019-24 PMID: 15381690
  11. Function of alternative splicing.
    Gene. 2005 Jan 3;344:1-20 PMID: 15656968
  12. Discovery of novel splice forms and functional analysis of cancer-specific alternative splicing in human expressed sequences.
    Nucleic Acids Res. 2003 Oct 1;31(19):5635-43 PMID: 14500827
  13. Calcium-regulated intramembrane proteolysis of the RAGE receptor.
    Biochem Biophys Res Commun. 2008 May 23;370(1):1-5 PMID: 18355449
  14. The evolving roles of alternative splicing.
    Curr Opin Struct Biol. 2004 Jun;14(3):273-82 PMID: 15193306
  15. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance.
    Trends Biochem Sci. 1998 Jun;23(6):198-9 PMID: 9644970
  16. RAGE drives the development of glomerulosclerosis and implicates podocyte activation in the pathogenesis of diabetic nephropathy.
    Am J Pathol. 2003 Apr;162(4):1123-37 PMID: 12651605
  17. Widespread production of novel soluble protein isoforms by alternative splicing removal of transmembrane anchoring domains.
    FEBS Lett. 2003 Dec 18;555(3):572-8 PMID: 14675776
  18. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts.
    Nat Med. 1998 Sep;4(9):1025-31 PMID: 9734395
  19. cDNA cloning of a novel secreted isoform of the human receptor for advanced glycation end products and characterization of cells co-expressing cell-surface scavenger receptors and Swedish mutant amyloid precursor protein.
    Brain Res Mol Brain Res. 1999 Aug 25;71(2):159-70 PMID: 10521570
  20. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides.
    Cell. 1999 Jun 25;97(7):889-901 PMID: 10399917
  21. Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury.
    Biochem J. 2003 Mar 15;370(Pt 3):1097-109 PMID: 12495433
  22. Diabetic vascular disease: it's all the RAGE.
    Antioxid Redox Signal. 2005 Nov-Dec;7(11-12):1588-600 PMID: 16356122
  23. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases.
    Nature. 2000 May 18;405(6784):354-60 PMID: 10830965
  24. Receptor for advanced glycation end products mediates inflammation and enhanced expression of tissue factor in vasculature of diabetic apolipoprotein E-null mice.
    Arterioscler Thromb Vasc Biol. 2001 Jun;21(6):905-10 PMID: 11397695
  25. Central role of RAGE-dependent neointimal expansion in arterial restenosis.
    J Clin Invest. 2003 Apr;111(7):959-72 PMID: 12671045
  26. RAGE modulates vascular inflammation and atherosclerosis in a murine model of type 2 diabetes.
    Atherosclerosis. 2006 Mar;185(1):70-7 PMID: 16076470
  27. Guidelines for human gene nomenclature.
    Genomics. 2002 Apr;79(4):464-70 PMID: 11944974
  28. Tissue-specific expression patterns of the RAGE receptor and its soluble forms--a result of regulated alternative splicing?
    Biochim Biophys Acta. 2003 Oct 20;1630(1):1-6 PMID: 14580673
  29. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease.
    Nature. 1996 Aug 22;382(6593):685-91 PMID: 8751438
  30. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice.
    Am J Pathol. 2001 Aug;159(2):513-25 PMID: 11485910
  31. Developmental expression of the receptor for advanced glycation end-products (RAGE) and its response to hyperoxia in the neonatal rat lung.
    BMC Dev Biol. 2007 Mar 07;7:15 PMID: 17343756
  32. Conserved and species-specific alternative splicing in mammalian genomes.
    BMC Evol Biol. 2007 Dec 22;7:249 PMID: 18154685
  33. Splice variants of the receptor for advanced glycosylation end products (RAGE) in human brain.
    Neurosci Lett. 2005 Jan 3;373(1):67-72 PMID: 15555779
  34. Circulating soluble receptor for advanced glycation end products is inversely associated with glycemic control and S100A12 protein.
    J Clin Endocrinol Metab. 2006 Nov;91(11):4628-34 PMID: 16926247
  35. Assay validation and biological variation of serum receptor for advanced glycation end-products.
    Ann Clin Biochem. 2008 Sep;45(Pt 5):518-9 PMID: 18753428
  36. Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in nondiabetic men.
    Arterioscler Thromb Vasc Biol. 2005 May;25(5):1032-7 PMID: 15731496
  37. Plasma level of endogenous secretory RAGE is associated with components of the metabolic syndrome and atherosclerosis.
    Arterioscler Thromb Vasc Biol. 2005 Dec;25(12):2587-93 PMID: 16224056
  38. Decreased endogenous secretory advanced glycation end product receptor in type 1 diabetic patients: its possible association with diabetic vascular complications.
    Diabetes Care. 2005 Nov;28(11):2716-21 PMID: 16249545
  39. A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10).
    FASEB J. 2008 Oct;22(10):3716-27 PMID: 18603587
  40. Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42.
    J Biol Chem. 2008 Dec 5;283(49):34457-68 PMID: 18922799
  41. Decreased plasma levels of soluble receptor for advanced glycation end-products in patients with essential hypertension.
    J Hypertens. 2005 Sep;23(9):1725-9 PMID: 16093918
Article Info
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
Abbr.
FASEB J
ISSN
1530-6860
Published
2009-06-00
Epub
2009-00-22
Pages
1766-74
Language
English
Region
United States
NLM ID
8804484
PMCID
PMC2698653
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com