Home LiteratureArticle Details
PMID: 17517690 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

A common polymorphism decreases low-density lipoprotein receptor exon 12 splicing efficiency and associates with increased cholesterol.

Human molecular genetics ·Vol. 16 ·No. 14 ·2007-07-15 ·Pages 1765-72

Zhu H, Tucker HM, Grear KE, Simpson JF, Manning AK, Cupples LA, Estus S

Abstract

Single nucleotide polymorphisms (SNPs) that alter exon splicing efficiency are an emerging class of functional genetic variants. Since mutations in low-density lipoprotein receptor (LDLR) are a primary cause of familial hypercholesterolemia, we evaluated whether LDLR SNPs may alter splicing efficiency and cholesterol homeostasis. A SNP within LDLR exon 12, rs688, was identified in silico as neutralizing a putative exon splicing enhancer. Studies in human liver samples established that this SNP was associated with significantly decreased LDLR exon 12 splicing efficiency in women in vivo. In vitro minigene splicing studies qualitatively replicated these in vivo results and demonstrated that rs688 specifically modulates splicing efficiency. These effects on splicing may be physiologically relevant because the presence of the rs688 minor allele associates with increased total and LDL-cholesterol in female members of the Framingham Offspring Study. The largest rs688-associated cholesterol differences were observed in pre-menopausal women. In summary, these studies identify an LDLR SNP present in approximately 60% of Caucasians that is associated with significant 10% increases in total and LDL-cholesterol in pre-menopausal women.

MeSH Terms
Adult Alleles Amino Acid Sequence Base Sequence Cholesterol/metabolism Exons Female Humans Liver/metabolism Male Middle Aged Molecular Sequence Data Polymorphism, Genetic Polymorphism, Single Nucleotide Receptors, LDL/genetics,physiology Sex Factors
Chemicals
Receptors, LDL Cholesterol
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Zhu Haiyan
Department of Physiology and Sanders-Brown Center on Aging, 800 S. Limestone Street, University of Kentucky, Lexington, KY 40536-0230, USA.
Tucker H Michael
Grear Karrie E
Simpson James F
Manning Alisa K
Cupples L Adrienne
Estus Steven
References (34)
34 references, click to expand
  1. A common mutation of low-density lipoprotein receptor gene is associated with essential hypertension among Japanese.
    J Hum Hypertens. 2001 Feb;15(2):125-30 PMID: 11317192
  2. Analysis of alternatively spliced isoforms of human LDL receptor mRNA.
    Clin Chim Acta. 2006 Nov;373(1-2):151-7 PMID: 16828075
  3. Listening to silence and understanding nonsense: exonic mutations that affect splicing.
    Nat Rev Genet. 2002 Apr;3(4):285-98 PMID: 11967553
  4. Common haplotypes in five genes influence genetic variance of LDL and HDL cholesterol in the general population.
    Hum Mol Genet. 2002 Jun 1;11(12):1477-85 PMID: 12023990
  5. Predictive identification of exonic splicing enhancers in human genes.
    Science. 2002 Aug 9;297(5583):1007-13 PMID: 12114529
  6. A secreted soluble form of ApoE receptor 2 acts as a dominant-negative receptor and inhibits Reelin signaling.
    EMBO J. 2002 Nov 15;21(22):5996-6004 PMID: 12426372
  7. Structure of the LDL receptor extracellular domain at endosomal pH.
    Science. 2002 Dec 20;298(5602):2353-8 PMID: 12459547
  8. Structural biology. LDL receptor's beta-propeller displaces LDL.
    Science. 2002 Dec 20;298(5602):2337-9 PMID: 12493900
  9. Alternative pre-mRNA splicing and neuronal function.
    Prog Mol Subcell Biol. 2003;31:187-216 PMID: 12494767
  10. Glutamate regulates caveolin expression in rat hippocampal neurons.
    J Neurosci Res. 2003 Apr 15;72(2):185-90 PMID: 12671992
  11. ESEfinder: A web resource to identify exonic splicing enhancers.
    Nucleic Acids Res. 2003 Jul 1;31(13):3568-71 PMID: 12824367
  12. Joe Goldstein and Mike Brown: from cholesterol homeostasis to new paradigms in membrane biology.
    Trends Cell Biol. 2003 Oct;13(10):534-9 PMID: 14507481
  13. Mechanisms of alternative pre-messenger RNA splicing.
    Annu Rev Biochem. 2003;72:291-336 PMID: 12626338
  14. Primary hypercholesterolemia: genetic causes and treatment of five monogenic disorders.
    Expert Rev Cardiovasc Ther. 2003 May;1(1):107-19 PMID: 15030301
  15. Haplotypes and SNPs in 13 lipid-relevant genes explain most of the genetic variance in high-density lipoprotein and low-density lipoprotein cholesterol.
    Hum Mol Genet. 2004 May 15;13(10):993-1004 PMID: 15044381
  16. RESCUE-ESE identifies candidate exonic splicing enhancers in vertebrate exons.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W187-90 PMID: 15215377
  17. PupaSNP Finder: a web tool for finding SNPs with putative effect at transcriptional level.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W242-8 PMID: 15215388
  18. The role of common single-nucleotide polymorphisms on exon 9 and exon 12 skipping in nonmutated CFTR alleles.
    Hum Mutat. 2004 Aug;24(2):120-9 PMID: 15241793
  19. Single nucleotide polymorphism-based validation of exonic splicing enhancers.
    PLoS Biol. 2004 Sep;2(9):E268 PMID: 15340491
  20. The Lebanese allele at the low density lipoprotein receptor locus. Nonsense mutation produces truncated receptor that is retained in endoplasmic reticulum.
    J Biol Chem. 1987 Jan 5;262(1):401-10 PMID: 3025214
  21. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  22. Human LDL receptor gene: HincII polymorphism detected by gene amplification.
    Nucleic Acids Res. 1988 Jul 25;16(14B):7215 PMID: 2900502
  23. Molecular genetics of the LDL receptor gene in familial hypercholesterolemia.
    Hum Mutat. 1992;1(6):445-66 PMID: 1301956
  24. Exonic splicing enhancer motif recognized by human SC35 under splicing conditions.
    Mol Cell Biol. 2000 Feb;20(3):1063-71 PMID: 10629063
  25. Requirement of Sp1 and estrogen receptor alpha interaction in 17beta-estradiol-mediated transcriptional activation of the low density lipoprotein receptor gene expression.
    Endocrinology. 2001 Apr;142(4):1546-53 PMID: 11250935
  26. Effects of gender and menopausal status on the association of apolipoprotein E phenotype with plasma lipoprotein levels. Results from the Framingham Offspring Study.
    Arterioscler Thromb. 1994 Jul;14(7):1105-13 PMID: 8018666
  27. Aggregated amyloid-beta protein induces cortical neuronal apoptosis and concomitant "apoptotic" pattern of gene induction.
    J Neurosci. 1997 Oct 15;17(20):7736-45 PMID: 9315895
  28. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins.
    Genes Dev. 1998 Jul 1;12(13):1998-2012 PMID: 9649504
  29. Association and linkage of LDLR gene variation with variation in plasma low density lipoprotein cholesterol.
    J Hum Genet. 1998;43(3):153-9 PMID: 9747026
  30. Disruption of exonic splicing enhancer elements is the principal cause of exon skipping associated with seven nonsense or missense alleles of NF1.
    Hum Mutat. 2004 Dec;24(6):491-501 PMID: 15523642
  31. Linking C5 deficiency to an exonic splicing enhancer mutation.
    J Immunol. 2005 Apr 1;174(7):4172-7 PMID: 15778377
  32. LDL receptor family: isolation, production, and ligand binding analysis.
    Methods. 2005 Jun;36(2):109-16 PMID: 15893937
  33. The switch in alternative splicing of cyclic AMP-response element modulator protein CREM{tau}2{alpha} (activator) to CREM{alpha} (repressor) in human myometrial cells is mediated by SRp40.
    J Biol Chem. 2005 Oct 14;280(41):34521-9 PMID: 16103121
  34. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1.
    Nat Genet. 2002 Apr;30(4):377-84 PMID: 11925564
Article Info
Journal
Human molecular genetics
Abbr.
Hum Mol Genet
ISSN
0964-6906
Published
2007-07-15
Epub
2007-00-21
Pages
1765-72
Language
English
Region
England
NLM ID
9208958
PMCID
PMC2361133
Subset
IM
Grants
NIA NIH HHS · T32AG000242 · United States
NHLBI NIH HHS · N01-HC-25195 · United States
NIA NIH HHS · T32 AG000242 · United States
NIA NIH HHS · R01 AG026147-01A2 · United States
NIA NIH HHS · R01AG026147 · United States
NIA NIH HHS · R01 AG026147 · United States
NHLBI NIH HHS · N01HC25195 · United States
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: [email protected]