Medical College of Wisconsin
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Martin Bienengraeber PhD

Associate Professor

Institution: Medical College of Wisconsin
Department: Anesthesiology
Division: Research


Research Experience

  • Ischemic Preconditioning, Myocardial
  • Mitochondria
  • near infrared light
  • Publications

  • Complex I and ATP synthase mediate membrane depolarization and matrix acidification by isoflurane in mitochondria. (Pravdic D, Hirata N, Barber L, Sedlic F, Bosnjak ZJ, Bienengraeber M) Eur J Pharmacol 2012 Sep 5;690(1-3):149-57 PMID 22796646
  • Isoflurane differentially modulates mitochondrial reactive oxygen species production via forward versus reverse electron transport flow: implications for preconditioning. (Hirata N, Shim YH, Pravdic D, Lohr NL, Pratt PF Jr, Weihrauch D, Kersten JR, Warltier DC, Bosnjak ZJ, Bienengraeber M) Anesthesiology 2011 Sep;115(3):531-40 PMID 21862887
  • Partial restoration of the long QT syndrome associated KCNQ1 A341V mutant by the KCNE1 β-subunit. (Mikuni I, Torres CG, Bienengraeber MW, Kwok WM) Biochim Biophys Acta 2011 Dec;1810(12):1285-93 PMID 21854832
  • Endothelial-cardiomyocyte crosstalk enhances pharmacological cardioprotection. (Leucker TM, Bienengraeber M, Muravyeva M, Baotic I, Weihrauch D, Brzezinska AK, Warltier DC, Kersten JR, Pratt PF Jr) J Mol Cell Cardiol 2011 Nov;51(5):803-11 PMID 21791217
  • Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. (Camara AK, Bienengraeber M, Stowe DF) Front Physiol 2011;2:13 PMID 21559063
  • Isoflurane preconditioning elicits competent endogenous mechanisms of protection from oxidative stress in cardiomyocytes derived from human embryonic stem cells. (Sepac A, Sedlic F, Si-Tayeb K, Lough J, Duncan SA, Bienengraeber M, Park F, Kim J, Bosnjak ZJ) Anesthesiology 2010 Oct;113(4):906-16 PMID 20823757
  • Monitoring mitochondrial electron fluxes using NAD(P)H-flavoprotein fluorometry reveals complex action of isoflurane on cardiomyocytes. (Sedlic F, Pravdic D, Hirata N, Mio Y, Sepac A, Camara AK, Wakatsuki T, Bosnjak ZJ, Bienengraeber M) Biochim Biophys Acta 2010 Oct;1797(10):1749-58 PMID 20646994
  • Mitochondrial depolarization underlies delay in permeability transition by preconditioning with isoflurane: roles of ROS and Ca2+. (Sedlic F, Sepac A, Pravdic D, Camara AK, Bienengraeber M, Brzezinska AK, Wakatsuki T, Bosnjak ZJ) Am J Physiol Cell Physiol 2010 Aug;299(2):C506-15 PMID 20519447
  • Isoflurane protects cardiomyocytes and mitochondria by immediate and cytosol-independent action at reperfusion. (Pravdic D, Mio Y, Sedlic F, Pratt PF, Warltier DC, Bosnjak ZJ, Bienengraeber M) Br J Pharmacol 2010 May;160(2):220-32 PMID 20423337
  • KATP channel subunits in rat dorsal root ganglia: alterations by painful axotomy. (Zoga V, Kawano T, Liang MY, Bienengraeber M, Weihrauch D, McCallum B, Gemes G, Hogan Q, Sarantopoulos C) Mol Pain 2010;6:6 PMID 20102598
  • Isoflurane postconditioning protects against reperfusion injury by preventing mitochondrial permeability transition by an endothelial nitric oxide synthase-dependent mechanism. (Ge ZD, Pravdic D, Bienengraeber M, Pratt PF Jr, Auchampach JA, Gross GJ, Kersten JR, Warltier DC) Anesthesiology 2010 Jan;112(1):73-85 PMID 19996950
  • Anesthetic-induced preconditioning delays opening of mitochondrial permeability transition pore via protein Kinase C-epsilon-mediated pathway. (Pravdic D, Sedlic F, Mio Y, Vladic N, Bienengraeber M, Bosnjak ZJ) Anesthesiology 2009 Aug;111(2):267-74 PMID 19568162
  • Xenon preconditioning: the role of prosurvival signaling, mitochondrial permeability transition and bioenergetics in rats. (Mio Y, Shim YH, Richards E, Bosnjak ZJ, Pagel PS, Bienengraeber M) Anesth Analg 2009 Mar;108(3):858-66 PMID 19224794
  • Role of heat shock protein 90 and endothelial nitric oxide synthase during early anesthetic and ischemic preconditioning. (Amour J, Brzezinska AK, Weihrauch D, Billstrom AR, Zielonka J, Krolikowski JG, Bienengraeber MW, Warltier DC, Pratt PF Jr, Kersten JR) Anesthesiology 2009 Feb;110(2):317-25 PMID 19194158
  • Near infrared light protects cardiomyocytes from hypoxia and reoxygenation injury by a nitric oxide dependent mechanism. (Zhang R, Mio Y, Pratt PF, Lohr N, Warltier DC, Whelan HT, Zhu D, Jacobs ER, Medhora M, Bienengraeber M) J Mol Cell Cardiol 2009 Jan;46(1):4-14 PMID 18930064
  • Age-related attenuation of isoflurane preconditioning in human atrial cardiomyocytes: roles for mitochondrial respiration and sarcolemmal adenosine triphosphate-sensitive potassium channel activity. (Mio Y, Bienengraeber MW, Marinovic J, Gutterman DD, Rakic M, Bosnjak ZJ, Stadnicka A) Anesthesiology 2008 Apr;108(4):612-20 PMID 18362592
  • Role for SUR2A ED domain in allosteric coupling within the K(ATP) channel complex. (Karger AB, Park S, Reyes S, Bienengraeber M, Dyer RB, Terzic A, Alekseev AE) J Gen Physiol 2008 Mar;131(3):185-96 PMID 18299394
  • Role of sarcolemmal ATP-sensitive potassium channel in oxidative stress-induced apoptosis: mitochondrial connection. (Marinovic J, Ljubkovic M, Stadnicka A, Bosnjak ZJ, Bienengraeber M) Am J Physiol Heart Circ Physiol 2008 Mar;294(3):H1317-25 PMID 18192220
  • Effective pharmacotherapy against oxidative injury: alternative utility of an ATP-sensitive potassium channel opener. (Ozcan C, Terzic A, Bienengraeber M) J Cardiovasc Pharmacol 2007 Oct;50(4):411-8 PMID 18049309
  • The A3 adenosine receptor agonist CP-532,903 [N6-(2,5-dichlorobenzyl)-3'-aminoadenosine-5'-N-methylcarboxamide] protects against myocardial ischemia/reperfusion injury via the sarcolemmal ATP-sensitive potassium channel. (Wan TC, Ge ZD, Tampo A, Mio Y, Bienengraeber MW, Tracey WR, Gross GJ, Kwok WM, Auchampach JA) J Pharmacol Exp Ther 2008 Jan;324(1):234-43 PMID 17906066
  • Volatile anesthetic-induced cardiac preconditioning. (Stadnicka A, Marinovic J, Ljubkovic M, Bienengraeber MW, Bosnjak ZJ) J Anesth 2007;21(2):212-9 PMID 17458651
  • Isoflurane preconditioning uncouples mitochondria and protects against hypoxia-reoxygenation. (Ljubkovic M, Mio Y, Marinovic J, Stadnicka A, Warltier DC, Bosnjak ZJ, Bienengraeber M) Am J Physiol Cell Physiol 2007 May;292(5):C1583-90 PMID 17215328
  • Targeted expression of Kir6.2 in mitochondria confers protection against hypoxic stress. (Ljubkovic M, Marinovic J, Fuchs A, Bosnjak ZJ, Bienengraeber M) J Physiol 2006 Nov 15;577(Pt 1):17-29 PMID 16959852
  • Mechanism of cardiac sarcolemmal adenosine triphosphate-sensitive potassium channel activation by isoflurane in a heterologous expression system. (Bienengraeber M, Warltier DC, Bosnjak ZJ, Stadnicka A) Anesthesiology 2006 Sep;105(3):534-40 PMID 16931986
  • Extracellular signal-regulated kinases trigger isoflurane preconditioning concomitant with upregulation of hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression in rats. (Wang C, Weihrauch D, Schwabe DA, Bienengraeber M, Warltier DC, Kersten JR, Pratt PF Jr, Pagel PS) Anesth Analg 2006 Aug;103(2):281-8, table of contents PMID 16861403
  • Cardioprotection by volatile anesthetics: new applications for old drugs? (Pratt PF Jr, Wang C, Weihrauch D, Bienengraeber MW, Kersten JR, Pagel PS, Warltier DC) Curr Opin Anaesthesiol 2006 Aug;19(4):397-403 PMID 16829721
  • Kv1.5 channelopathy due to KCNA5 loss-of-function mutation causes human atrial fibrillation. (Olson TM, Alekseev AE, Liu XK, Park S, Zingman LV, Bienengraeber M, Sattiraju S, Ballew JD, Jahangir A, Terzic A) Hum Mol Genet 2006 Jul 15;15(14):2185-91 PMID 16772329
  • The influence of B-cell lymphoma 2 protein, an antiapoptotic regulator of mitochondrial permeability transition, on isoflurane-induced and ischemic postconditioning in rabbits. (Wang C, Neff DA, Krolikowski JG, Weihrauch D, Bienengraeber M, Warltier DC, Kersten JR, Pagel PS) Anesth Analg 2006 May;102(5):1355-60 PMID 16632808
  • Inhibition of glycogen synthase kinase enhances isoflurane-induced protection against myocardial infarction during early reperfusion in vivo. (Pagel PS, Krolikowski JG, Neff DA, Weihrauch D, Bienengraeber M, Kersten JR, Warltier DC) Anesth Analg 2006 May;102(5):1348-54 PMID 16632807
  • Impact of in vivo preconditioning by isoflurane on adenosine triphosphate-sensitive potassium channels in the rat heart: lasting modulation of nucleotide sensitivity during early memory period. (Stadnicka A, Marinovic J, Bienengraeber M, Bosnjak ZJ) Anesthesiology 2006 Mar;104(3):503-10 PMID 16508398
  • Role of Erk1/2, p70s6K, and eNOS in isoflurane-induced cardioprotection during early reperfusion in vivo. (Krolikowski JG, Weihrauch D, Bienengraeber M, Kersten JR, Warltier DC, Pagel PS) Can J Anaesth 2006 Feb;53(2):174-82 PMID 16434759
  • Inhibition of mitochondrial permeability transition enhances isoflurane-induced cardioprotection during early reperfusion: the role of mitochondrial KATP channels. (Krolikowski JG, Bienengraeber M, Weihrauch D, Warltier DC, Kersten JR, Pagel PS) Anesth Analg 2005 Dec;101(6):1590-6 PMID 16301224
  • Isoflurane inhibits cardiac myocyte apoptosis during oxidative and inflammatory stress by activating Akt and enhancing Bcl-2 expression. (Jamnicki-Abegg M, Weihrauch D, Pagel PS, Kersten JR, Bosnjak ZJ, Warltier DC, Bienengraeber MW) Anesthesiology 2005 Nov;103(5):1006-14 PMID 16249675
  • Morphine enhances isoflurane-induced postconditioning against myocardial infarction: the role of phosphatidylinositol-3-kinase and opioid receptors in rabbits. (Weihrauch D, Krolikowski JG, Bienengraeber M, Kersten JR, Warltier DC, Pagel PS) Anesth Analg 2005 Oct;101(4):942-9, table of contents PMID 16192500
  • Deletion of mtDNA disrupts mitochondrial function and structure, but not biogenesis. (Holmuhamedov E, Jahangir A, Bienengraeber M, Lewis LD, Terzic A) Mitochondrion 2003 Aug;3(1):13-9 PMID 16120340
  • Role of endothelial nitric oxide synthase as a trigger and mediator of isoflurane-induced delayed preconditioning in rabbit myocardium. (Chiari PC, Bienengraeber MW, Weihrauch D, Krolikowski JG, Kersten JR, Warltier DC, Pagel PS) Anesthesiology 2005 Jul;103(1):74-83 PMID 15983459
  • Cardioprotection by volatile anesthetics. (Bienengraeber MW, Weihrauch D, Kersten JR, Pagel PS, Warltier DC) Vascul Pharmacol 2005 Apr-May;42(5-6):243-52 PMID 15922257
  • Isoflurane protects against myocardial infarction during early reperfusion by activation of phosphatidylinositol-3-kinase signal transduction: evidence for anesthetic-induced postconditioning in rabbits. (Chiari PC, Bienengraeber MW, Pagel PS, Krolikowski JG, Kersten JR, Warltier DC) Anesthesiology 2005 Jan;102(1):102-9 PMID 15618793
  • ABCC9 mutations identified in human dilated cardiomyopathy disrupt catalytic KATP channel gating. (Bienengraeber M, Olson TM, Selivanov VA, Kathmann EC, O'Cochlain F, Gao F, Karger AB, Ballew JD, Hodgson DM, Zingman LV, Pang YP, Alekseev AE, Terzic A) Nat Genet 2004 Apr;36(4):382-7 PMID 15034580
  • Mitochondrial tolerance to stress impaired in failing heart. (Ozcan C, Bienengraeber M, Hodgson DM, Mann DL, Terzic A) J Mol Cell Cardiol 2003 Sep;35(9):1161-6 PMID 12967639
  • Stable transfection of UCP1 confers resistance to hypoxia/reoxygenation in a heart-derived cell line. (Bienengraeber M, Ozcan C, Terzic A) J Mol Cell Cardiol 2003 Jul;35(7):861-5 PMID 12818577
  • Identity and function of cardiac K(ATP) channels. (Bienengraeber M, Hodgson DM, Zingman LV, Alekseev AE, Terzic A) J Mol Cell Cardiol 2003 May;35(5):433-5 PMID 12738225
  • Cellular remodeling in heart failure disrupts K(ATP) channel-dependent stress tolerance. (Hodgson DM, Zingman LV, Kane GC, Perez-Terzic C, Bienengraeber M, Ozcan C, Gumina RJ, Pucar D, O'Coclain F, Mann DL, Alekseev AE, Terzic A) EMBO J 2003 Apr 15;22(8):1732-42 PMID 12682006
  • Bacterial enterotoxins are associated with resistance to colon cancer. (Pitari GM, Zingman LV, Hodgson DM, Alekseev AE, Kazerounian S, Bienengraeber M, Hajnóczky G, Terzic A, Waldman SA) Proc Natl Acad Sci U S A 2003 Mar 4;100(5):2695-9 PMID 12594332
  • Kir6.2 is required for adaptation to stress. (Zingman LV, Hodgson DM, Bast PH, Kane GC, Perez-Terzic C, Gumina RJ, Pucar D, Bienengraeber M, Dzeja PP, Miki T, Seino S, Alekseev AE, Terzic A) Proc Natl Acad Sci U S A 2002 Oct 1;99(20):13278-83 PMID 12271142
  • Suppression of human tumor cell proliferation through mitochondrial targeting. (Holmuhamedov E, Lewis L, Bienengraeber M, Holmuhamedova M, Jahangir A, Terzic A) FASEB J 2002 Jul;16(9):1010-6 PMID 12087062
  • Tandem function of nucleotide binding domains confers competence to sulfonylurea receptor in gating ATP-sensitive K+ channels. (Zingman LV, Hodgson DM, Bienengraeber M, Karger AB, Kathmann EC, Alekseev AE, Terzic A) J Biol Chem 2002 Apr 19;277(16):14206-10 PMID 11825892
  • Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation. (Ozcan C, Bienengraeber M, Dzeja PP, Terzic A) Am J Physiol Heart Circ Physiol 2002 Feb;282(2):H531-9 PMID 11788400
  • Signaling in channel/enzyme multimers: ATPase transitions in SUR module gate ATP-sensitive K+ conductance. (Zingman LV, Alekseev AE, Bienengraeber M, Hodgson D, Karger AB, Dzeja PP, Terzic A) Neuron 2001 Aug 2;31(2):233-45 PMID 11502255
  • Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. (Carrasco AJ, Dzeja PP, Alekseev AE, Pucar D, Zingman LV, Abraham MR, Hodgson D, Bienengraeber M, Puceat M, Janssen E, Wieringa B, Terzic A) Proc Natl Acad Sci U S A 2001 Jun 19;98(13):7623-8 PMID 11390963
  • Role of intrahelical arginine residues in functional properties of uncoupling protein (UCP1). (Echtay KS, Bienengraeber M, Klingenberg M) Biochemistry 2001 May 1;40(17):5243-8 PMID 11318647
  • ATPase activity of the sulfonylurea receptor: a catalytic function for the KATP channel complex. (Bienengraeber M, Alekseev AE, Abraham MR, Carrasco AJ, Moreau C, Vivaudou M, Dzeja PP, Terzic A) FASEB J 2000 Oct;14(13):1943-52 PMID 11023978
  • Site-directed mutagenesis identifies residues in uncoupling protein (UCP1) involved in three different functions. (Echtay KS, Winkler E, Bienengraeber M, Klingenberg M) Biochemistry 2000 Mar 28;39(12):3311-7 PMID 10727223
  • Structure-function relationship in UCP1. (Klingenberg M, Echtay KS, Bienengraeber M, Winkler E, Huang SG) Int J Obes Relat Metab Disord 1999 Jun;23 Suppl 6:S24-9 PMID 10454117
  • In the uncoupling protein (UCP-1) His-214 is involved in the regulation of purine nucleoside triphosphate but not diphosphate binding. (Echtay KS, Bienengraeber M, Winkler E, Klingenberg M) J Biol Chem 1998 Sep 18;273(38):24368-74 PMID 9733725
  • H+ transport by uncoupling protein (UCP-1) is dependent on a histidine pair, absent in UCP-2 and UCP-3. (Bienengraeber M, Echtay KS, Klingenberg M) Biochemistry 1998 Jan 6;37(1):3-8 PMID 9453747
  • Mutagenesis of the uncoupling protein of brown adipose tissue. Neutralization Of E190 largely abolishes pH control of nucleotide binding. (Echtay KS, Bienengraeber M, Klingenberg M) Biochemistry 1997 Jul 8;36(27):8253-60 PMID 9204870
  • Grants and Awards

  • Mechanisms of Photobiomodulation in Myocardial Reperfusion Injury (#9206271 06/15/2010 - 05/31/2015) Sponsor: NIH Heart Lung and Blood Institute