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miRNA in the Regulation of Ion Channel/Transporter Expression

Zhiguo Wang

10.1002/cphy.c110002

Source: Volume 3, Issue 2, April 2013

Published online: April 2013

Full Article on Wiley Online Library



Abstract

Ion channels and transporters are expressed in every living cell, where they participate in controlling a plethora of biological processes and physiological functions, such as excitation of cells in response to stimulation, electrical activities of cells, excitation‐contraction coupling, cellular osmolarity, and even cell growth and death. Alterations of ion channels/transporters can have profound impacts on the cellular physiology associated with these proteins. Expression of ion channels/transporters is tightly regulated and expression deregulation can trigger abnormal processes, leading to pathogenesis, the channelopathies. While transcription factors play a critical role in controlling the transcriptome of ion channels/transporters at the transcriptional level by acting on the 5′‐flanking region of the genes, microribonucleic acids (miRNAs), a newly discovered class of regulators in the gene network, are also crucial for expression regulation at the posttranscriptional level through binding to the 3′untranslated region of the genes. These small noncoding RNAs fine tune expression of genes involved in a wide variety of cellular processes. Recent studies revealed the role of miRNAs in regulating expression of ion channels/transporters and the associated physiological functions. miRNAs can target ion channel genes to alter cardiac excitability (conduction, repolarization, and automaticity) and affect arrhythmogenic potential of heart. They can modulate circadian rhythm, pain threshold, neuroadaptation to alcohol, brain edema, etc., through targeting ion channel genes in the neuronal systems. miRNAs can also control cell growth and tumorigenesis by acting on the relevant ion channel genes. Future studies are expected to rapidly increase to unravel a new repertoire of ion channels/transporters for miRNA regulation. © 2013 American Physiological Society. Compr Physiol 3:599‐653, 2013.

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Figure 1. Figure 1.

The human genome project has been completed years ago. Only less than 2% of all transcribed bases of the entire human genome constitutes the genetic sequence encoding proteins and the rest of 98% accounting for approximately 70% of all genes carry the sequences for ribonucleic acids (RNAs) not encoding a polypeptide chain that was used to be considered for many years “junk DNA” of no physiologic function. We now known that “junk DNA” encodes nonprotein‐coding RNAs that are involved in determining the expression of protein‐coding genes by regulating the activity of that less than 2% of the genome. These ncRNAs include microRNAs (miRNAs): to date, more than 1200 human miRNAs have been identified. Gene expression regulation occurs at least at two levels: transcriptional and posttranscriptional levels. For transcriptional regulation, transcription factors bind to the respective cis‐acting elements, the protein‐binding motifs, in the 5’‐flanking region of a gene to switch on or off the transcription of the targeted gene to define the transcriptome of cells. For posttranscriptional regulation, miRNAs bind to the respective binding sites in the 3′UTR of target genes to aid to define the proteome of cells.
Figure 2. Figure 2.

Genomic organization and classification of miRNAs. TSS, transcription start site.
Figure 3. Figure 3.

Schematic illustration of miRNA biogenesis pathway (see detailed description in text) and the sites for miRNA interference along the pathway. The arrows and the numbers indicate the sites of miRNAi action. RNA Pol II, RNA polymerase II; TF, transcription factor; intergenic miRNAs, miRNA‐coding genes located in between protein‐coding genes; intronic miRNAs, miRNA‐coding genes located within introns of their host protein‐coding genes; mirtron, the intron within a protein‐coding gene (the host gene) which contains miRNA sequences; Drosha, the nuclear RNase III ribonuclease; Dicer, cytoplasmic RNase III ribonuclease; pri‐miRNA, primary miRNA; pre‐miRNA, precursor miRNA; RISC, RNA‐induced silencing complex. represents the site for interfering transcription of endogenous miRNAs by altering TFs; represents the site for interfering miRNA biogenesis by silencing Drosha; represents the site for interfering miRNA biogenesis by manipulating exportin‐5 to influence the translocation of miRNA from nucleus to cytoplasm; represents the site for interfering miRNA biogenesis by knocking down or knocking out Dicer; represents the site for interfering miRNA action by inhibiting RISC; represents the site for interfering miRNA action and stability by targeting mature miRNA using antisense [such as anti‐miRNA antisense oligonucleotides, multiple‐target anti‐miRNA antisense oligonucleotides , microribonucleic acid (miRNA) sponge, antagomiR, and locked nucleic acid‐antimiR; and represents the site for interfering miRNA action in a gene‐specific manner by using miR‐Mimic and miR‐Mask technologies (see Section “Manipulating miRNA by miRNA interference”).
Figure 4. Figure 4.

Upper panel: the sequence motifs within a microribonucleic acid (miRNA) (miR‐1 as an example) important to its function (see Section “Mechanisms of miRNA action” for detail). Seed site is highlighted in yellow, cleavage site in green, and 3'supplementary and 3'compensatory site in red. Centered site is indicated by the region below a blue bar. Lower panel: an example of seed‐site targeting of the GJA1 gene by miR‐1 and centered site targeting of the VAMP1 gene by miR‐1.
Figure 5. Figure 5.

Procedures for experimental validation of ion channel genes as targets for microribonucleic acids.
Figure 6. Figure 6.

Schematic illustration of a cardiac action potential, the underlying ion currents in five sequential phases (0‐4), the protein subunits carrying the currents, and the genes encoding the subunits.
Figure 7. Figure 7.

The miR‐1 seed family members and the base pairing between miR‐1 and its target genes GJA1 (encoding connexin 43 for Ij current), and between miR‐1 and KCNJ2 (encoding Kir2.1 for IK1). The seed sites are highlighted in yellow. Note the seed‐site and cleavage‐site base pairing between miR‐1 and GJA1, and only the seed‐site base pairing between miR‐1 and KCNJ2.
Figure 8. Figure 8.

Schematic diagram showing miR‐1 targeting of GJA1/Cx43/Ij and KCNJ2/ Kir2.1/IK1, leading to ischemic arrhythmias in myocardial infarction.
Figure 9. Figure 9.

The miR‐26 seed family members and miR‐26a:KCNJ2 base pairing and miR‐26b:KCNJ2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity between miR‐26 and KCNJ2.
Figure 10. Figure 10.

Schematic diagram showing the upregulation of KCNJ2/Kir2.1/IK1 due to a relief of repression with miR‐26 downregulation and the consequent promotion of atrial fibrillation.
Figure 11. Figure 11.

The miR‐133 seed family members and miR‐133:KCNQ1 base pairing and miR‐133:KCNH2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity for both.
Figure 12. Figure 12.

Schematic diagram showing the repression of KCNH2/h‐erg1/IKr and KCNQ1/KvLQT1/IKs by miR‐133.
Figure 13. Figure 13.

Schematic diagram showing the repression of KCNH2/h‐erg1/IKr and KCNQ1/KvLQT1/IKs by miR‐133.
Figure 14. Figure 14.

Diagram showing the steps miR‐1 causes arrhythmias via disrupting intracellular Ca2+ handling process. miR‐1 produces translational inhibition of the B56α regulatory subunit of protein phosphatase PP2A, which in turn causes hyperphosphorylation of LTCC (L‐type Ca2+ channels) RyR2 (ryanodine receptor 2) by CaMKII, enhancing DAD (delayed afterdepolarization) and EAD (early afterdepolarization) leading to arrhythmogenesis. This mechanism likely works with the conduction slowing mechanism to promote arrhythmogenesis.
Figure 15. Figure 15.

The miR‐328 seed family members and miR‐328:CACNA1C base pairing. The seed site is highlighted in yellow. Note the seed‐site complementarity between miR‐328 and CACNA1C.
Figure 16. Figure 16.

The miR‐26 seed family members and miR‐26a:CACNA1C base pairing and miR‐26b:CACNA1C base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity between miR‐26 and CACNA1C.
Figure 17. Figure 17.

Diagram showing how miR‐26a is involved in the regulation of intrinsic circadian rhythm. CLOCK, circadian locomoter output cycles kaput; CREB, cAMP‐response element‐binding protein; LTCC, L‐type Ca2+ channels.
Figure 18. Figure 18.

The miR‐9 seed family members and miR‐9:KCNMA1 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity and cleavage site complementarity between miR‐9 and KCNMA1.
Figure 19. Figure 19.

Ion channels known to be involved in regulation of pain threshold and their alterations in expression in a mice line with conditional deletion of Dicer to produce overall downregulation of microribonucleic acids (miRNAs). Removal of miRNAs paradoxically downregulates Nax1.x and TRPCx, possibly via altering expression of transcription factors (TFs) that regulate these channel genes at the transcriptional level. Nav1.x: mainly referring to Nav1.7, Nav1.8, and Nav1.9; TRPCx: mainly referring to TRPC3 and TRPC6.
Figure 20. Figure 20.

The miR‐320 seed family members and miR‐320a:AQP1 base pairing and miR‐320a:AQP4 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity and centered site complementarity between miR‐320a and AQP1.
Figure 21. Figure 21.

The miR‐204 seed family members and miR‐204/miR‐211:TGFBR2 base pairing and miR‐204/miR‐211:SNAIL2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity and cleavage site complementarity between miR‐204/miR‐211 and their target genes.
Figure 22. Figure 22.

Diagram showing how miR‐204/miR‐211 regulates epithelial function in the retinal pigment epithelium via indirectly modulating expression of claudins and Kir7.1 K+ channel genes by directly targeting the TGFBR2 and SNAIL2 genes. TER, transepithelial electrical resistance; TJ, tight junction.
Figure 23. Figure 23.

The miR‐124 seed family members and miR‐124:FOXA2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site, cleavage site, and centered site complementarity between miR‐124a and FOXA2.
Figure 24. Figure 24.

Diagram showing how miR‐124 regulates intracellular Ca2+ signaling in the pancreatic β‐cells via indirectly modulating Kir6.2 and SUR1 expression by directly targeting the FOXA2 gene.
Figure 25. Figure 25.

The miR‐34 seed family members and detailed juxtaposition of miR‐34 with h‐eag1 3′UTR and h‐erg1 3′UTR. The seed sites are highlighted in yellow. Note the seed‐site complementarity and cleavage site complementarity between miR‐34a/miR‐34b/miR‐34c and their target genes.
Figure 26. Figure 26.

Schematic illustration of the p53‐miR‐34‐E2F1‐h‐eag1/h‐erg1

signaling pathway as a mechanism for oncogenic upregulation of h‐eag1/h‐erg1 and the growth‐stimulating action of h‐eag1/h‐erg1 in cancer cells.
Figure 27. Figure 27.

Schematic depiction of roles of microribonucleic acids in regulating ion channel genes and the associated pathophysiological processes. AMI, acute myocardial infarction, CH, cardiac hypertrophy, HF, heart failure; AF, atrial fibrillation; OS, oxidative stress. Dashlines indicate downregulation and solid lines indicate upregulation.


Figure 1.

The human genome project has been completed years ago. Only less than 2% of all transcribed bases of the entire human genome constitutes the genetic sequence encoding proteins and the rest of 98% accounting for approximately 70% of all genes carry the sequences for ribonucleic acids (RNAs) not encoding a polypeptide chain that was used to be considered for many years “junk DNA” of no physiologic function. We now known that “junk DNA” encodes nonprotein‐coding RNAs that are involved in determining the expression of protein‐coding genes by regulating the activity of that less than 2% of the genome. These ncRNAs include microRNAs (miRNAs): to date, more than 1200 human miRNAs have been identified. Gene expression regulation occurs at least at two levels: transcriptional and posttranscriptional levels. For transcriptional regulation, transcription factors bind to the respective cis‐acting elements, the protein‐binding motifs, in the 5’‐flanking region of a gene to switch on or off the transcription of the targeted gene to define the transcriptome of cells. For posttranscriptional regulation, miRNAs bind to the respective binding sites in the 3′UTR of target genes to aid to define the proteome of cells.



Figure 2.

Genomic organization and classification of miRNAs. TSS, transcription start site.



Figure 3.

Schematic illustration of miRNA biogenesis pathway (see detailed description in text) and the sites for miRNA interference along the pathway. The arrows and the numbers indicate the sites of miRNAi action. RNA Pol II, RNA polymerase II; TF, transcription factor; intergenic miRNAs, miRNA‐coding genes located in between protein‐coding genes; intronic miRNAs, miRNA‐coding genes located within introns of their host protein‐coding genes; mirtron, the intron within a protein‐coding gene (the host gene) which contains miRNA sequences; Drosha, the nuclear RNase III ribonuclease; Dicer, cytoplasmic RNase III ribonuclease; pri‐miRNA, primary miRNA; pre‐miRNA, precursor miRNA; RISC, RNA‐induced silencing complex. represents the site for interfering transcription of endogenous miRNAs by altering TFs; represents the site for interfering miRNA biogenesis by silencing Drosha; represents the site for interfering miRNA biogenesis by manipulating exportin‐5 to influence the translocation of miRNA from nucleus to cytoplasm; represents the site for interfering miRNA biogenesis by knocking down or knocking out Dicer; represents the site for interfering miRNA action by inhibiting RISC; represents the site for interfering miRNA action and stability by targeting mature miRNA using antisense [such as anti‐miRNA antisense oligonucleotides, multiple‐target anti‐miRNA antisense oligonucleotides , microribonucleic acid (miRNA) sponge, antagomiR, and locked nucleic acid‐antimiR; and represents the site for interfering miRNA action in a gene‐specific manner by using miR‐Mimic and miR‐Mask technologies (see Section “Manipulating miRNA by miRNA interference”).



Figure 4.

Upper panel: the sequence motifs within a microribonucleic acid (miRNA) (miR‐1 as an example) important to its function (see Section “Mechanisms of miRNA action” for detail). Seed site is highlighted in yellow, cleavage site in green, and 3'supplementary and 3'compensatory site in red. Centered site is indicated by the region below a blue bar. Lower panel: an example of seed‐site targeting of the GJA1 gene by miR‐1 and centered site targeting of the VAMP1 gene by miR‐1.



Figure 5.

Procedures for experimental validation of ion channel genes as targets for microribonucleic acids.



Figure 6.

Schematic illustration of a cardiac action potential, the underlying ion currents in five sequential phases (0‐4), the protein subunits carrying the currents, and the genes encoding the subunits.



Figure 7.

The miR‐1 seed family members and the base pairing between miR‐1 and its target genes GJA1 (encoding connexin 43 for Ij current), and between miR‐1 and KCNJ2 (encoding Kir2.1 for IK1). The seed sites are highlighted in yellow. Note the seed‐site and cleavage‐site base pairing between miR‐1 and GJA1, and only the seed‐site base pairing between miR‐1 and KCNJ2.



Figure 8.

Schematic diagram showing miR‐1 targeting of GJA1/Cx43/Ij and KCNJ2/ Kir2.1/IK1, leading to ischemic arrhythmias in myocardial infarction.



Figure 9.

The miR‐26 seed family members and miR‐26a:KCNJ2 base pairing and miR‐26b:KCNJ2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity between miR‐26 and KCNJ2.



Figure 10.

Schematic diagram showing the upregulation of KCNJ2/Kir2.1/IK1 due to a relief of repression with miR‐26 downregulation and the consequent promotion of atrial fibrillation.



Figure 11.

The miR‐133 seed family members and miR‐133:KCNQ1 base pairing and miR‐133:KCNH2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity for both.



Figure 12.

Schematic diagram showing the repression of KCNH2/h‐erg1/IKr and KCNQ1/KvLQT1/IKs by miR‐133.



Figure 13.

Schematic diagram showing the repression of KCNH2/h‐erg1/IKr and KCNQ1/KvLQT1/IKs by miR‐133.



Figure 14.

Diagram showing the steps miR‐1 causes arrhythmias via disrupting intracellular Ca2+ handling process. miR‐1 produces translational inhibition of the B56α regulatory subunit of protein phosphatase PP2A, which in turn causes hyperphosphorylation of LTCC (L‐type Ca2+ channels) RyR2 (ryanodine receptor 2) by CaMKII, enhancing DAD (delayed afterdepolarization) and EAD (early afterdepolarization) leading to arrhythmogenesis. This mechanism likely works with the conduction slowing mechanism to promote arrhythmogenesis.



Figure 15.

The miR‐328 seed family members and miR‐328:CACNA1C base pairing. The seed site is highlighted in yellow. Note the seed‐site complementarity between miR‐328 and CACNA1C.



Figure 16.

The miR‐26 seed family members and miR‐26a:CACNA1C base pairing and miR‐26b:CACNA1C base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity between miR‐26 and CACNA1C.



Figure 17.

Diagram showing how miR‐26a is involved in the regulation of intrinsic circadian rhythm. CLOCK, circadian locomoter output cycles kaput; CREB, cAMP‐response element‐binding protein; LTCC, L‐type Ca2+ channels.



Figure 18.

The miR‐9 seed family members and miR‐9:KCNMA1 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity and cleavage site complementarity between miR‐9 and KCNMA1.



Figure 19.

Ion channels known to be involved in regulation of pain threshold and their alterations in expression in a mice line with conditional deletion of Dicer to produce overall downregulation of microribonucleic acids (miRNAs). Removal of miRNAs paradoxically downregulates Nax1.x and TRPCx, possibly via altering expression of transcription factors (TFs) that regulate these channel genes at the transcriptional level. Nav1.x: mainly referring to Nav1.7, Nav1.8, and Nav1.9; TRPCx: mainly referring to TRPC3 and TRPC6.



Figure 20.

The miR‐320 seed family members and miR‐320a:AQP1 base pairing and miR‐320a:AQP4 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity and centered site complementarity between miR‐320a and AQP1.



Figure 21.

The miR‐204 seed family members and miR‐204/miR‐211:TGFBR2 base pairing and miR‐204/miR‐211:SNAIL2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site complementarity and cleavage site complementarity between miR‐204/miR‐211 and their target genes.



Figure 22.

Diagram showing how miR‐204/miR‐211 regulates epithelial function in the retinal pigment epithelium via indirectly modulating expression of claudins and Kir7.1 K+ channel genes by directly targeting the TGFBR2 and SNAIL2 genes. TER, transepithelial electrical resistance; TJ, tight junction.



Figure 23.

The miR‐124 seed family members and miR‐124:FOXA2 base pairing. The seed sites are highlighted in yellow. Note the seed‐site, cleavage site, and centered site complementarity between miR‐124a and FOXA2.



Figure 24.

Diagram showing how miR‐124 regulates intracellular Ca2+ signaling in the pancreatic β‐cells via indirectly modulating Kir6.2 and SUR1 expression by directly targeting the FOXA2 gene.



Figure 25.

The miR‐34 seed family members and detailed juxtaposition of miR‐34 with h‐eag1 3′UTR and h‐erg1 3′UTR. The seed sites are highlighted in yellow. Note the seed‐site complementarity and cleavage site complementarity between miR‐34a/miR‐34b/miR‐34c and their target genes.



Figure 26.

Schematic illustration of the p53‐miR‐34‐E2F1‐h‐eag1/h‐erg1

signaling pathway as a mechanism for oncogenic upregulation of h‐eag1/h‐erg1 and the growth‐stimulating action of h‐eag1/h‐erg1 in cancer cells.



Figure 27.

Schematic depiction of roles of microribonucleic acids in regulating ion channel genes and the associated pathophysiological processes. AMI, acute myocardial infarction, CH, cardiac hypertrophy, HF, heart failure; AF, atrial fibrillation; OS, oxidative stress. Dashlines indicate downregulation and solid lines indicate upregulation.

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Further Reading
 1.Latronico MV, Condorelli G. MicroRNAs and cardiac pathology. Nat Rev Cardiol 6: 419‐429, 2009.
 2.Latronico MV, Condorelli G. RNA silencing: Small RNA‐mediated posttranscriptional regulation of mRNA and the implications for heart electropathophysiology. J Cardiovasc Electrophysiol 20: 230‐237, 2009.
 3.Wang Z. MicroRNA‐interference Technologies. New York: Springer‐Verlag, 2009.
 4.Wang Z. The role of microRNA in cardiac excitability. J Cardiovasc Pharmacol 56: 460‐470, 2010.
 5.Wang Z. MicroRNAs and Cardiovascular Disease. Bentham Science, 2010.

Further Reading

Latronico MV, Condorelli G. MicroRNAs and cardiac pathology. Nat Rev Cardiol 6: 419–429, 2009.

Latronico MV, Condorelli G. RNA silencing: small RNA-mediated posttranscriptional regulation of mRNA and the implications for heart electropathophysiology. J Cardiovasc Electrophysiol 20: 230–237, 2009.

Wang Z. The role of microRNA in cardiac excitability. J Cardiovasc Pharmacol 56: 460–470, 2010.

Wang Z. MicroRNAs and cardiovascular disease. Bentham Science, 2010.

Wang Z. MicroRNA-interference technologies. New York: Springer-Verlag, 2009.

 

 

 

 

 

 

 

 

Corrigendum

miRNA in the Regulation of Ion Channel/Transporter Expression, Zhiguo Wang, Comprehensive Physiology 2:599-653, 2013.

It has come to our attention that four of the references (226, 227, 425 and 426) listed in the article were retracted from the literature prior to publication of this article and should have been removed from the final version of the article.  The author apologizes for this error and draws your attention to the fact that the article content related to these references may be unreliable.


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Article Title: miRNA in the Regulation of Ion Channel/Transporter Expression
 

How to Cite

Zhiguo Wang. miRNA in the Regulation of Ion Channel/Transporter Expression. Compr Physiol 2013, 3: 599-653. doi: 10.1002/cphy.c110002