P-glycoprotein (Mdr1a/1b) and breast cancer resistance protein (Bcrp) decrease the uptake of hydrophobic alkyl triphenylphosphonium cations by the brain
Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumu...
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| Published in | Biochimica et biophysica acta Vol. 1830; no. 6; pp. 3458 - 3465 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.06.2013
Elsevier Pub. Co |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0304-4165 0006-3002 1872-8006 1872-8006 1878-2434 |
| DOI | 10.1016/j.bbagen.2013.02.005 |
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| Abstract | Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs.
To discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp.
There was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls.
Efflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver.
These findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain.
► Brain accumulation of triphenylphosphonium cations is decreased by ABC transporters. ► ABC-transporter inactivation increases brain uptake of triphenylphosphonium cations. ► Bypassing ABC transporters may increase the effectiveness of mitochondrial therapies. |
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| AbstractList | > Brain accumulation of triphenylphosphonium cations is decreased by ABC transporters. > ABC-transporter inactivation increases brain uptake of triphenylphosphonium cations. > Bypassing ABC transporters may increase the effectiveness of mitochondrial therapies. Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs.To discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp.There was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls.Efflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver.These findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain. BACKGROUND: Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs. METHODS: To discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp. RESULTS: There was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls. CONCLUSION: Efflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver. GENERAL SIGNIFICANCE: These findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain. Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs.BACKGROUNDMitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs.To discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp.METHODSTo discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp.There was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls.RESULTSThere was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls.Efflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver.CONCLUSIONEfflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver.These findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain.GENERAL SIGNIFICANCEThese findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain. Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs. To discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp. There was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls. Efflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver. These findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain. ► Brain accumulation of triphenylphosphonium cations is decreased by ABC transporters. ► ABC-transporter inactivation increases brain uptake of triphenylphosphonium cations. ► Bypassing ABC transporters may increase the effectiveness of mitochondrial therapies. ► Brain accumulation of triphenylphosphonium cations is decreased by ABC transporters. ► ABC-transporter inactivation increases brain uptake of triphenylphosphonium cations. ► Bypassing ABC transporters may increase the effectiveness of mitochondrial therapies. Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are effective within the brain. One approach to deliver pharmacophores is by conjugation to the lipophilic triphenylphosphonium (TPP) cation that accumulates in mitochondria driven by the membrane potential. While this approach has delivered TPP-conjugated compounds to the brain, the amounts taken up are lower than by other organs. To discover why uptake of hydrophobic TPP compounds by the brain is relatively poor, we assessed the role of the P-glycoprotein (Mdr1a/b) and breast cancer resistance protein (Bcrp) ATP binding cassette (ABC) transporters, which drive the efflux of lipophilic compounds from the brain thereby restricting the uptake of lipophilic drugs. We used a triple transgenic mouse model lacking two isoforms of P-glycoprotein (Mdr1a/1b) and the Bcrp. There was a significant increase in the uptake into the brain of two hydrophobic TPP compounds, MitoQ and MitoF, in the triple transgenics following intra venous (IV) administration compared to control mice. Greater amounts of the hydrophobic TPP compounds were also retained in the liver of transgenic mice compared to controls. The uptake into the heart, white fat, muscle and kidneys was comparable between the transgenic mice and controls. Efflux of hydrophobic TPP compounds by ABC transporters contributes to their lowered uptake into the brain and liver. These findings suggest that strategies to bypass ABC transporters in the BBB will enhance delivery of mitochondria-targeted antioxidants, probes and pharmacophores to the brain. |
| Author | Smith, Robin A.J. Porteous, Carolyn M. Menon, David K. Murphy, Michael P. Aigbirhio, Franklin I. |
| Author_xml | – sequence: 1 givenname: Carolyn M. surname: Porteous fullname: Porteous, Carolyn M. organization: Department of Chemistry, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand – sequence: 2 givenname: David K. surname: Menon fullname: Menon, David K. organization: Division of Anaesthesia, University of Cambridge, Box 93, Addenbrooke's Hospital, Hills Road, Cambridge CB2 0QQ, UK – sequence: 3 givenname: Franklin I. surname: Aigbirhio fullname: Aigbirhio, Franklin I. organization: Wolfson Brain Imaging Centre, Department of Clinical Neurosciences, University of Cambridge, Addenbrooke's Hospital, Hills Road, Cambridge CB2 0QQ, UK – sequence: 4 givenname: Robin A.J. surname: Smith fullname: Smith, Robin A.J. organization: Department of Chemistry, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand – sequence: 5 givenname: Michael P. surname: Murphy fullname: Murphy, Michael P. email: mpm@mrc-mbu.cam.ac.uk organization: MRC Mitochondrial Biology Unit, Hills Road, Cambridge, CB2 0XY, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23454352$$D View this record in MEDLINE/PubMed |
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Biophys. Acta doi: 10.1016/j.bbagen.2010.06.001 |
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| Snippet | Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that are... BACKGROUND: Mitochondrial dysfunction contributes to degenerative neurological disorders, consequently there is a need for mitochondria-targeted therapies that... > Brain accumulation of triphenylphosphonium cations is decreased by ABC transporters. > ABC-transporter inactivation increases brain uptake of... ► Brain accumulation of triphenylphosphonium cations is decreased by ABC transporters. ► ABC-transporter inactivation increases brain uptake of... |
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| SubjectTerms | ABC transporters animal models Animals antioxidants ATP Binding Cassette Transporter, Subfamily B - genetics ATP Binding Cassette Transporter, Subfamily B - metabolism ATP Binding Cassette Transporter, Subfamily G, Member 2 ATP-Binding Cassette Sub-Family B Member 4 ATP-Binding Cassette Transporters - genetics ATP-Binding Cassette Transporters - metabolism Blood-Brain Barrier - metabolism Blood–brain barrier brain breast neoplasms cations drugs heart Heterocyclic Compounds - pharmacokinetics Heterocyclic Compounds - pharmacology hydrophobicity kidneys Lipophilic cation liver Liver - metabolism membrane potential Mice Mice, Knockout Mitochondria Mitochondrial Diseases - drug therapy Mitochondrial Diseases - genetics Mitochondrial Diseases - metabolism MitoQ muscles Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism neurodegenerative diseases Organophosphorus Compounds - pharmacokinetics Organophosphorus Compounds - pharmacology Organoselenium Compounds - pharmacokinetics Organoselenium Compounds - pharmacology pharmacology transgenic animals white adipose tissue |
| Title | P-glycoprotein (Mdr1a/1b) and breast cancer resistance protein (Bcrp) decrease the uptake of hydrophobic alkyl triphenylphosphonium cations by the brain |
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