Mechanisms that match ATP supply to demand in cardiac pacemaker cells during high ATP demand
The spontaneous action potential (AP) firing rate of sinoatrial node cells (SANCs) involves high-throughput signaling via Ca(2+)-calmodulin activated adenylyl cyclases (AC), cAMP-mediated protein kinase A (PKA), and Ca(2+)/calmodulin-dependent protein kinase II (CaMKII)-dependent phosphorylation of...
Saved in:
| Published in: | American journal of physiology. Heart and circulatory physiology Vol. 304; no. 11; p. H1428 |
|---|---|
| Main Authors: | , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
01.06.2013
|
| Subjects: | |
| ISSN: | 1522-1539, 1522-1539 |
| Online Access: | Get more information |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | The spontaneous action potential (AP) firing rate of sinoatrial node cells (SANCs) involves high-throughput signaling via Ca(2+)-calmodulin activated adenylyl cyclases (AC), cAMP-mediated protein kinase A (PKA), and Ca(2+)/calmodulin-dependent protein kinase II (CaMKII)-dependent phosphorylation of SR Ca(2+) cycling and surface membrane ion channel proteins. When the throughput of this signaling increases, e.g., in response to β-adrenergic receptor activation, the resultant increase in spontaneous AP firing rate increases the demand for ATP. We hypothesized that an increase of ATP production to match the increased ATP demand is achieved via a direct effect of increased mitochondrial Ca(2+) (Ca(2+)m) and an indirect effect via enhanced Ca(2+)-cAMP/PKA-CaMKII signaling to mitochondria. To increase ATP demand, single isolated rabbit SANCs were superfused by physiological saline at 35 ± 0.5°C with isoproterenol, or by phosphodiesterase or protein phosphatase inhibition. We measured cytosolic and mitochondrial Ca(2+) and flavoprotein fluorescence in single SANC, and we measured cAMP, ATP, and O₂ consumption in SANC suspensions. Although the increase in spontaneous AP firing rate was accompanied by an increase in O₂ consumption, the ATP level and flavoprotein fluorescence remained constant, indicating that ATP production had increased. Both Ca(2+)m and cAMP increased concurrently with the increase in AP firing rate. When Ca(2+)m was reduced by Ru360, the increase in spontaneous AP firing rate in response to isoproterenol was reduced by 25%. Thus, both an increase in Ca(2+)m and an increase in Ca(2+) activated cAMP-PKA-CaMKII signaling regulate the increase in ATP supply to meet ATP demand above the basal level. |
|---|---|
| AbstractList | The spontaneous action potential (AP) firing rate of sinoatrial node cells (SANCs) involves high-throughput signaling via Ca(2+)-calmodulin activated adenylyl cyclases (AC), cAMP-mediated protein kinase A (PKA), and Ca(2+)/calmodulin-dependent protein kinase II (CaMKII)-dependent phosphorylation of SR Ca(2+) cycling and surface membrane ion channel proteins. When the throughput of this signaling increases, e.g., in response to β-adrenergic receptor activation, the resultant increase in spontaneous AP firing rate increases the demand for ATP. We hypothesized that an increase of ATP production to match the increased ATP demand is achieved via a direct effect of increased mitochondrial Ca(2+) (Ca(2+)m) and an indirect effect via enhanced Ca(2+)-cAMP/PKA-CaMKII signaling to mitochondria. To increase ATP demand, single isolated rabbit SANCs were superfused by physiological saline at 35 ± 0.5°C with isoproterenol, or by phosphodiesterase or protein phosphatase inhibition. We measured cytosolic and mitochondrial Ca(2+) and flavoprotein fluorescence in single SANC, and we measured cAMP, ATP, and O₂ consumption in SANC suspensions. Although the increase in spontaneous AP firing rate was accompanied by an increase in O₂ consumption, the ATP level and flavoprotein fluorescence remained constant, indicating that ATP production had increased. Both Ca(2+)m and cAMP increased concurrently with the increase in AP firing rate. When Ca(2+)m was reduced by Ru360, the increase in spontaneous AP firing rate in response to isoproterenol was reduced by 25%. Thus, both an increase in Ca(2+)m and an increase in Ca(2+) activated cAMP-PKA-CaMKII signaling regulate the increase in ATP supply to meet ATP demand above the basal level.The spontaneous action potential (AP) firing rate of sinoatrial node cells (SANCs) involves high-throughput signaling via Ca(2+)-calmodulin activated adenylyl cyclases (AC), cAMP-mediated protein kinase A (PKA), and Ca(2+)/calmodulin-dependent protein kinase II (CaMKII)-dependent phosphorylation of SR Ca(2+) cycling and surface membrane ion channel proteins. When the throughput of this signaling increases, e.g., in response to β-adrenergic receptor activation, the resultant increase in spontaneous AP firing rate increases the demand for ATP. We hypothesized that an increase of ATP production to match the increased ATP demand is achieved via a direct effect of increased mitochondrial Ca(2+) (Ca(2+)m) and an indirect effect via enhanced Ca(2+)-cAMP/PKA-CaMKII signaling to mitochondria. To increase ATP demand, single isolated rabbit SANCs were superfused by physiological saline at 35 ± 0.5°C with isoproterenol, or by phosphodiesterase or protein phosphatase inhibition. We measured cytosolic and mitochondrial Ca(2+) and flavoprotein fluorescence in single SANC, and we measured cAMP, ATP, and O₂ consumption in SANC suspensions. Although the increase in spontaneous AP firing rate was accompanied by an increase in O₂ consumption, the ATP level and flavoprotein fluorescence remained constant, indicating that ATP production had increased. Both Ca(2+)m and cAMP increased concurrently with the increase in AP firing rate. When Ca(2+)m was reduced by Ru360, the increase in spontaneous AP firing rate in response to isoproterenol was reduced by 25%. Thus, both an increase in Ca(2+)m and an increase in Ca(2+) activated cAMP-PKA-CaMKII signaling regulate the increase in ATP supply to meet ATP demand above the basal level. The spontaneous action potential (AP) firing rate of sinoatrial node cells (SANCs) involves high-throughput signaling via Ca(2+)-calmodulin activated adenylyl cyclases (AC), cAMP-mediated protein kinase A (PKA), and Ca(2+)/calmodulin-dependent protein kinase II (CaMKII)-dependent phosphorylation of SR Ca(2+) cycling and surface membrane ion channel proteins. When the throughput of this signaling increases, e.g., in response to β-adrenergic receptor activation, the resultant increase in spontaneous AP firing rate increases the demand for ATP. We hypothesized that an increase of ATP production to match the increased ATP demand is achieved via a direct effect of increased mitochondrial Ca(2+) (Ca(2+)m) and an indirect effect via enhanced Ca(2+)-cAMP/PKA-CaMKII signaling to mitochondria. To increase ATP demand, single isolated rabbit SANCs were superfused by physiological saline at 35 ± 0.5°C with isoproterenol, or by phosphodiesterase or protein phosphatase inhibition. We measured cytosolic and mitochondrial Ca(2+) and flavoprotein fluorescence in single SANC, and we measured cAMP, ATP, and O₂ consumption in SANC suspensions. Although the increase in spontaneous AP firing rate was accompanied by an increase in O₂ consumption, the ATP level and flavoprotein fluorescence remained constant, indicating that ATP production had increased. Both Ca(2+)m and cAMP increased concurrently with the increase in AP firing rate. When Ca(2+)m was reduced by Ru360, the increase in spontaneous AP firing rate in response to isoproterenol was reduced by 25%. Thus, both an increase in Ca(2+)m and an increase in Ca(2+) activated cAMP-PKA-CaMKII signaling regulate the increase in ATP supply to meet ATP demand above the basal level. |
| Author | Lyashkov, Alexey E Spurgeon, Harold A Yaniv, Yael Lakatta, Edward G Ziman, Bruce D |
| Author_xml | – sequence: 1 givenname: Yael surname: Yaniv fullname: Yaniv, Yael organization: Laboratory of Cardiovascular Science, Gerontology Research Center, Intramural Research Program, National Institute on Aging, National Institutes of Health, Baltimore, MD 21224, USA – sequence: 2 givenname: Harold A surname: Spurgeon fullname: Spurgeon, Harold A – sequence: 3 givenname: Bruce D surname: Ziman fullname: Ziman, Bruce D – sequence: 4 givenname: Alexey E surname: Lyashkov fullname: Lyashkov, Alexey E – sequence: 5 givenname: Edward G surname: Lakatta fullname: Lakatta, Edward G |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23604710$$D View this record in MEDLINE/PubMed |
| BookMark | eNpNUMtKw0AUHaRiH_oFgszSTeo8M82yFKtCRRd1J4R5tZmaTOLMZNG_N9IKchfncs-Dw52CkW-9BeAWoznGnDzIQ1dZGdIcoSIv5gRhcgEmA0MyzGkx-rePwTTGA0KIi5xegTGhOWICown4fLW6kt7FJsJUyQQbmXQFl9t3GPuuq48wtdDYRnoDnYdaBuOkhp3Uw-3LBqhtXUdo-uD8HlZuf_KeHNfgcifraG_OOAMf68ft6jnbvD29rJabTDNKU6ZYgZm2imOFtWELzpUViuZ2x9FAUMEQxpjuLDJUEs4KJRZC5kQrQZASmMzA_Sm3C-13b2MqGxd_i0lv2z6WmOYcDVMsBundWdqrxpqyC66R4Vj-fYT8AExeZT4 |
| CitedBy_id | crossref_primary_10_1016_j_exger_2017_12_015 crossref_primary_10_1016_j_hlc_2025_04_084 crossref_primary_10_1016_j_hrthm_2014_05_037 crossref_primary_10_1016_j_ceca_2018_12_008 crossref_primary_10_3389_fphys_2017_00584 crossref_primary_10_5483_BMBRep_2015_48_12_061 crossref_primary_10_1007_s11302_014_9436_1 crossref_primary_10_1091_mbc_E17_01_0041 crossref_primary_10_1113_jphysiol_2013_265090 crossref_primary_10_1016_j_yjmcc_2015_07_024 crossref_primary_10_3389_fphys_2020_00163 crossref_primary_10_1007_s00395_015_0468_7 crossref_primary_10_3390_ijms19082173 crossref_primary_10_1161_JAHA_118_009775 crossref_primary_10_1161_JAHA_118_009289 crossref_primary_10_3389_fphys_2016_00419 crossref_primary_10_1007_s12012_024_09931_9 crossref_primary_10_3389_fphys_2021_634816 crossref_primary_10_1111_acel_12483 crossref_primary_10_1016_j_yjmcc_2023_10_007 crossref_primary_10_3389_fphar_2014_00058 crossref_primary_10_3390_cells10113106 |
| ContentType | Journal Article |
| DBID | CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1152/ajpheart.00969.2012 |
| DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed MEDLINE - Academic |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic MEDLINE |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | no_fulltext_linktorsrc |
| Discipline | Medicine Anatomy & Physiology |
| EISSN | 1522-1539 |
| ExternalDocumentID | 23604710 |
| Genre | Journal Article Research Support, N.I.H., Intramural |
| GrantInformation_xml | – fundername: Intramural NIH HHS |
| GroupedDBID | --- 23M 2WC 39C 4.4 53G 5GY 5VS 6J9 AAFWJ ABJNI ACBEA ACIWK ACPRK ADBBV AENEX AFRAH ALMA_UNASSIGNED_HOLDINGS BAWUL BKKCC BKOMP BTFSW CGR CUY CVF E3Z EBS ECM EIF EJD EMOBN F5P GX1 H13 ITBOX KQ8 NPM OK1 P2P PQQKQ RAP RHI RPL RPRKH TR2 UKR W8F WH7 WOQ XSW YSK ~02 7X8 |
| ID | FETCH-LOGICAL-c433t-b4914ceb51b1cd4855be7b36ef5014c37401113fe0d3a2549b787a62cb720b712 |
| IEDL.DBID | 7X8 |
| ISICitedReferencesCount | 29 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000319808200003&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 1522-1539 |
| IngestDate | Fri Jul 11 08:34:55 EDT 2025 Thu Apr 03 06:56:48 EDT 2025 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 11 |
| Keywords | bioenergetics pacemaker automaticity calcium-activated adenylyl cyclase |
| Language | English |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c433t-b4914ceb51b1cd4855be7b36ef5014c37401113fe0d3a2549b787a62cb720b712 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | http://doi.org/10.1152/ajpheart.00969.2012 |
| PMID | 23604710 |
| PQID | 1365050598 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_1365050598 pubmed_primary_23604710 |
| PublicationCentury | 2000 |
| PublicationDate | 2013-06-01 |
| PublicationDateYYYYMMDD | 2013-06-01 |
| PublicationDate_xml | – month: 06 year: 2013 text: 2013-06-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | American journal of physiology. Heart and circulatory physiology |
| PublicationTitleAlternate | Am J Physiol Heart Circ Physiol |
| PublicationYear | 2013 |
| References | 18356168 - J Biol Chem. 2008 May 23;283(21):14461-8 9161982 - J Physiol. 1997 May 1;500 ( Pt 3):643-51 19325782 - Int J Mol Sci. 2008 May;9(5):751-67 9733088 - J Bioenerg Biomembr. 1998 Jun;30(3):207-22 21276796 - J Mol Cell Cardiol. 2011 Oct;51(4):468-73 20201896 - Ann N Y Acad Sci. 2010 Feb;1188:133-42 12878477 - J Mol Cell Cardiol. 2003 Aug;35(8):905-13 1638717 - Circulation. 1992 Aug;86(2):494-503 16043637 - Circulation. 2005 Aug 2;112(5):674-82 2912189 - Am J Physiol. 1989 Jan;256(1 Pt 2):H265-74 18375388 - J Biol Chem. 2008 May 30;283(22):15063-71 22022409 - PLoS One. 2011;6(10):e25539 23459256 - PLoS One. 2013;8(2):e57079 23243207 - Circ Res. 2013 Feb 1;112(3):424-31 22886415 - Am J Physiol Heart Circ Physiol. 2012 Oct 15;303(8):H940-66 20547682 - J Physiol. 2010 Aug 15;588(Pt 16):2987-98 7537039 - Biochem Biophys Res Commun. 1995 Apr 6;209(1):213-7 3403540 - J Biol Chem. 1988 Aug 15;263(23):11498-503 17540702 - J Physiol. 2007 Aug 1;582(Pt 3):1195-203 21978991 - J Cardiovasc Pharmacol. 2011 Oct;58(4):339-44 22666369 - PLoS One. 2012;7(5):e37582 16778127 - Circ Res. 2006 Jul 21;99(2):172-82 23077656 - PLoS One. 2012;7(10):e47652 18599868 - Circ Res. 2008 Aug 1;103(3):279-88 3704638 - Science. 1986 May 30;232(4754):1121-3 7775334 - J Appl Physiol (1985). 1995 Mar;78(3):890-900 19345225 - J Mol Cell Cardiol. 2009 Jun;46(6):1027-36 19289071 - Biophys J. 2009 Mar 18;96(6):2466-78 21937057 - J Electrocardiol. 2011 Nov-Dec;44(6):626-34 16410283 - J Physiol. 2006 Mar 1;571(Pt 2):253-73 20203315 - Circ Res. 2010 Mar 5;106(4):659-73 17467631 - Heart Rhythm. 2007 May;4(5):619-26 21835182 - J Mol Cell Cardiol. 2011 Nov;51(5):740-8 10200426 - J Physiol. 1999 May 1;516 ( Pt 3):793-804 18276917 - Circ Res. 2008 Apr 11;102(7):761-9 22201686 - J Clin Invest. 2012 Jan;122(1):291-302 2309919 - Am J Physiol. 1990 Feb;258(2 Pt 2):H574-86 10974216 - Cardiovasc Res. 2000 Sep;47(4):658-87 19249308 - J Mol Cell Cardiol. 2009 Jun;46(6):891-901 7587239 - Crit Care Med. 1995 Oct;23(10):1726-33 17525366 - Circ Res. 2007 Jun 22;100(12):1723-31 |
| References_xml | – reference: 22886415 - Am J Physiol Heart Circ Physiol. 2012 Oct 15;303(8):H940-66 – reference: 19345225 - J Mol Cell Cardiol. 2009 Jun;46(6):1027-36 – reference: 19249308 - J Mol Cell Cardiol. 2009 Jun;46(6):891-901 – reference: 20201896 - Ann N Y Acad Sci. 2010 Feb;1188:133-42 – reference: 7775334 - J Appl Physiol (1985). 1995 Mar;78(3):890-900 – reference: 20547682 - J Physiol. 2010 Aug 15;588(Pt 16):2987-98 – reference: 19325782 - Int J Mol Sci. 2008 May;9(5):751-67 – reference: 16778127 - Circ Res. 2006 Jul 21;99(2):172-82 – reference: 9161982 - J Physiol. 1997 May 1;500 ( Pt 3):643-51 – reference: 19289071 - Biophys J. 2009 Mar 18;96(6):2466-78 – reference: 18599868 - Circ Res. 2008 Aug 1;103(3):279-88 – reference: 23459256 - PLoS One. 2013;8(2):e57079 – reference: 22201686 - J Clin Invest. 2012 Jan;122(1):291-302 – reference: 7537039 - Biochem Biophys Res Commun. 1995 Apr 6;209(1):213-7 – reference: 23243207 - Circ Res. 2013 Feb 1;112(3):424-31 – reference: 3403540 - J Biol Chem. 1988 Aug 15;263(23):11498-503 – reference: 12878477 - J Mol Cell Cardiol. 2003 Aug;35(8):905-13 – reference: 2912189 - Am J Physiol. 1989 Jan;256(1 Pt 2):H265-74 – reference: 17540702 - J Physiol. 2007 Aug 1;582(Pt 3):1195-203 – reference: 18375388 - J Biol Chem. 2008 May 30;283(22):15063-71 – reference: 23077656 - PLoS One. 2012;7(10):e47652 – reference: 2309919 - Am J Physiol. 1990 Feb;258(2 Pt 2):H574-86 – reference: 17467631 - Heart Rhythm. 2007 May;4(5):619-26 – reference: 1638717 - Circulation. 1992 Aug;86(2):494-503 – reference: 10974216 - Cardiovasc Res. 2000 Sep;47(4):658-87 – reference: 7587239 - Crit Care Med. 1995 Oct;23(10):1726-33 – reference: 10200426 - J Physiol. 1999 May 1;516 ( Pt 3):793-804 – reference: 18356168 - J Biol Chem. 2008 May 23;283(21):14461-8 – reference: 17525366 - Circ Res. 2007 Jun 22;100(12):1723-31 – reference: 21835182 - J Mol Cell Cardiol. 2011 Nov;51(5):740-8 – reference: 20203315 - Circ Res. 2010 Mar 5;106(4):659-73 – reference: 18276917 - Circ Res. 2008 Apr 11;102(7):761-9 – reference: 16043637 - Circulation. 2005 Aug 2;112(5):674-82 – reference: 21978991 - J Cardiovasc Pharmacol. 2011 Oct;58(4):339-44 – reference: 22022409 - PLoS One. 2011;6(10):e25539 – reference: 22666369 - PLoS One. 2012;7(5):e37582 – reference: 16410283 - J Physiol. 2006 Mar 1;571(Pt 2):253-73 – reference: 21276796 - J Mol Cell Cardiol. 2011 Oct;51(4):468-73 – reference: 21937057 - J Electrocardiol. 2011 Nov-Dec;44(6):626-34 – reference: 3704638 - Science. 1986 May 30;232(4754):1121-3 – reference: 9733088 - J Bioenerg Biomembr. 1998 Jun;30(3):207-22 |
| SSID | ssj0005763 |
| Score | 2.2311082 |
| Snippet | The spontaneous action potential (AP) firing rate of sinoatrial node cells (SANCs) involves high-throughput signaling via Ca(2+)-calmodulin activated adenylyl... |
| SourceID | proquest pubmed |
| SourceType | Aggregation Database Index Database |
| StartPage | H1428 |
| SubjectTerms | Adenosine Triphosphate - metabolism Animals Biological Clocks - physiology Calcium Signaling - physiology Calcium-Calmodulin-Dependent Protein Kinase Type 2 - physiology Cell Separation Cyclic AMP - metabolism Cyclic AMP-Dependent Protein Kinases - physiology Cytosol - metabolism Flavoproteins - metabolism Heart - physiology Heart Rate - physiology In Vitro Techniques Mitochondria, Heart - metabolism Mitochondria, Heart - physiology Myocardial Contraction - physiology Myocardium - cytology Myocardium - metabolism Myocytes, Cardiac - metabolism Myocytes, Cardiac - physiology Oxygen Consumption - physiology Phosphoprotein Phosphatases - antagonists & inhibitors Rabbits Receptors, Adrenergic, beta - physiology Respiratory Rate - physiology |
| Title | Mechanisms that match ATP supply to demand in cardiac pacemaker cells during high ATP demand |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/23604710 https://www.proquest.com/docview/1365050598 |
| Volume | 304 |
| WOSCitedRecordID | wos000319808200003&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1JS8NAFB7UinhxaV3qxgjibWySyXqSIhYvLT1U6EEIs4VWaVqbKPTf-94kpSdB8BLIMjBM3pv53voRcqfBRIiNBjPVZDHzVRCwhCuP6TARQoFFxI22ZBPRYBCPx8mwdrgVdVrlek-0G7WeK_SRdzAdC1nXkvhx8cmQNQqjqzWFxjZpcIAyKNXReNMtHLC0TbAHjMFAs5O66xDcd8T7AhmjywfE8FiwgpSUv2FMe9b0Dv87yyNyUKNM2q3E4phsmbxJWt0cLOzZit5Tm_dpHepNstevw-st8tY3WAg8LWYFLSeipABn1YR2R0NaIPvnipZzqs1M5JpOc6qsdCkKZjc8-zBLimGAglaljxQ7Idux1YgT8tp7Hj29sJp-gSmf85JJP3F9ZWTgSldpbCIjTSR5aDKMRSqOXH6uyzPjaC7QzpSg_CL0lIw8R0aud0p28nluzgnNhB9mgLwyeA3fBSLwktgRRiutHOPxNrldL2cK4o2TFbmZfxXpZkHb5Kz6J-mi6sORejx04Gx1Lv4w-pLsexWRBXPcK9LIQLnNNdlV3-W0WN5YuYHrYNj_AZaDzJ8 |
| linkProvider | ProQuest |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Mechanisms+that+match+ATP+supply+to+demand+in+cardiac+pacemaker+cells+during+high+ATP+demand&rft.jtitle=American+journal+of+physiology.+Heart+and+circulatory+physiology&rft.au=Yaniv%2C+Yael&rft.au=Spurgeon%2C+Harold+A&rft.au=Ziman%2C+Bruce+D&rft.au=Lyashkov%2C+Alexey+E&rft.date=2013-06-01&rft.issn=1522-1539&rft.eissn=1522-1539&rft.volume=304&rft.issue=11&rft.spage=H1428&rft_id=info:doi/10.1152%2Fajpheart.00969.2012&rft.externalDBID=NO_FULL_TEXT |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1522-1539&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1522-1539&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1522-1539&client=summon |