Cardioprotective trafficking of caveolin to mitochondria is Gi-protein dependent

Anesthesiology

Volumn 121, Issue 3, 2014, Pages 538-548

  Wang, Jiawan ^d   Schilling, Jan M ^a   Niesman, Ingrid R ^a   Headrick, John P ^c   Finley, J Cameron ^a   Kwan, Evan ^a   Patel, Piyush M ^a,b   Head, Brian P ^a,b   Roth, David M ^a,b   Yue, Yun ^d   Patel, Hemal H ^a,b  

^a University of California   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c GRIFFITH UNIVERSITY   (Australia)

^d CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALRETICULIN; CAVEOLIN; CAVEOLIN 1; CAVEOLIN 3; GLYCOGEN SYNTHASE KINASE 3BETA; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; ISOFLURANE; OXYGEN; PERTUSSIS TOXIN; PROHIBITIN; PROTEIN KINASE B; TRANSFERRIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA;

ANIMAL CELL; CAVEOLA; CELL FUNCTION; CELL STRUCTURE; CELL ULTRASTRUCTURE; CONFERENCE PAPER; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME PHOSPHORYLATION; HEART FUNCTION; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART MUSCLE CELL; HEART PROTECTION; ISCHEMIC PRECONDITIONING; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REPERFUSION INJURY; RESPIRATORY FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; METABOLISM; MYOCARDIAL REPERFUSION INJURY; PHYSIOLOGY; PROTEIN TRANSPORT; ULTRASTRUCTURE;

ANIMALS; CAVEOLAE; CAVEOLINS; GLYCOGEN SYNTHASE KINASE 3; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; ISOFLURANE; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MYOCARDIAL REPERFUSION INJURY; PERTUSSIS TOXIN; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84921656875     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000000295     Document Type: Conference Paper

References (48)

1. Hausenloy DJ, Yellon DM: Survival kinases in ischemic preconditioning and postconditioning. Cardiovasc Res 2006; 70:240-53.
2. Sanada S, Komuro I, Kitakaze M: Pathophysiology of myocardial reperfusion injury: Preconditioning, postconditioning, and translational aspects of protective measures. Am J Physiol Heart Circ Physiol 2011; 301:H1723-41.
3. Palade G: Fine structure of blood capillaries. J Appl Physiol 1953; 24:1424.
4. Pike LJ: Lipid rafts: Bringing order to chaos. J Lipid Res 2003; 44:655-67.
5. Parton RG, Way M, Zorzi N, Stang E: Caveolin-3 associates with developing T-tubules during muscle differentiation. J Cell Biol 1997; 136:137-54.
6. Chun M, Liyanage UK, Lisanti MP, Lodish HF: Signal transduction of a G protein-coupled receptor in caveolae: Colocalization of endothelin and its receptor with caveolin. Proc Natl Acad Sci U S A 1994; 91:11728-32.
7. Feron O, Balligand JL: Caveolins and the regulation of endothelial nitric oxide synthase in the heart. Cardiovasc Res 2006; 69:788-97.
8. Sargiacomo M, Scherer PE, Tang Z, Kübler E, Song KS, Sanders MC, Lisanti MP: Oligomeric structure of caveolin: Implications for caveolae membrane organization. Proc Natl Acad Sci U S A 1995; 92:9407-11.
9. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP: Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 1996; 271:15160-5.
10. Fujimoto T: Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol 1993; 120:1147-57.
11. Fujimoto T, Nakade S, Miyawaki A, Mikoshiba K, Ogawa K: Localization of inositol 1, 4, 5-trisphosphate receptor-like protein in plasmalemmal caveolae. J Cell Biol 1992; 119:1507-13.
12. Scriven DR, Klimek A, Lee KL, Moore ED: The molecular architecture of calcium microdomains in rat cardiomyocytes. Ann N Y Acad Sci 2002; 976:488-99.
13. Jones KA, Jiang X, Yamamoto Y, Yeung RS: Tuberin is a component of lipid rafts and mediates caveolin-1 localization: Role of TSC2 in post-Golgi transport. Exp Cell Res 2004; 295:512-24.
14. Peng Y, Akmentin W, Connelly MA, Lund-Katz S, Phillips MC, Williams DL: Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasma membrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein. Mol Biol Cell 2004; 15:384-96.
15. Lisanti MP, Scherer PE, Tang Z, Sargiacomo M: Caveolae, caveolin and caveolin-rich membrane domains: A signalling hypothesis. Trends Cell Biol 1994; 4:231-5.
16. Williams TM, Lisanti MP: The caveolin proteins. Genome Biol 2004; 5:214.
17. Steinberg SF, Brunton LL: Compartmentation of G proteincoupled signaling pathways in cardiac myocytes. Annu Rev Pharmacol Toxicol 2001; 41:751-73.
18. Cohen AW, Hnasko R, Schubert W, Lisanti MP: Role of caveolae and caveolins in health and disease. Physiol Rev 2004; 84:1341-79.
19. Li WP, Liu P, Pilcher BK, Anderson RG: Cell-specific targeting of caveolin-1 to caveolae, secretory vesicles, cytoplasm or mitochondria. J Cell Sci 2001; 114(Pt 7):1397-408.
20. Fridolfsson HN, Kawaraguchi Y, Ali SS, Panneerselvam M, Niesman IR, Finley JC, Kellerhals SE, Migita MY, Okada H, Moreno AL, Jennings M, Kidd MW, Bonds JA, Balijepalli RC, Ross RS, Patel PM, Miyanohara A, Chen Q, Lesnefsky EJ, Head BP, Roth DM, Insel PA, Patel HH: Mitochondrialocalized caveolin in adaptation to cellular stress and injury. FASEB J 2012; 26:4637-49.
21. Shaul PW, Anderson RG: Role of plasmalemmal caveolae in signal transduction. Am J Physiol 1998; 275(5 Pt 1):L843-51.
22. Patel HH, Murray F, Insel PA: Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 2008; 48:359-91.
23. Horikawa YT, Panneerselvam M, Kawaraguchi Y, Tsutsumi YM, Ali SS, Balijepalli RC, Murray F, Head BP, Niesman IR, Rieg T, Vallon V, Insel PA, Patel HH, Roth DM: Cardiac-specific overexpression of caveolin-3 attenuates cardiac hypertrophy and increases natriuretic peptide expression and signaling. J Am Coll Cardiol 2011; 57:2273-83.
24. Tsutsumi YM, Horikawa YT, Jennings MM, Kidd MW, Niesman IR, Yokoyama U, Head BP, Hagiwara Y, Ishikawa Y, Miyanohara A, Patel PM, Insel PA, Patel HH, Roth DM: Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 2008; 118:1979-88.
25. Tong H, Rockman HA, Koch WJ, Steenbergen C, Murphy E: G protein-coupled receptor internalization signaling is required for cardioprotection in ischemic preconditioning. Circ Res 2004; 94:1133-41.
26. Headrick JP, Willems L, Ashton KJ, Holmgren K, Peart J, Matherne GP: Ischaemic tolerance in aged mouse myocardium: The role of adenosine and effects of A1 adenosine receptor overexpression. J Physiol 2003; 549(Pt 3):823-33.
27. Reichelt ME, Willems L, Hack BA, Peart JN, Headrick JP: Cardiac and coronary function in the Langendorff-perfused mouse heart model. Exp Physiol 2009; 94:54-70.
28. Patel HH, Tsutsumi YM, Head BP, Niesman IR, Jennings M, Horikawa Y, Huang D, Moreno AL, Patel PM, Insel PA, Roth DM: Mechanisms of cardiac protection from ischemia/reperfusion injury: A role for caveolae and caveolin-1. FASEB J 2007; 21:1565-74.
29. Hausenloy DJ, Tsang A, Yellon DM: The reperfusion injury salvage kinase pathway: A common target for both ischemic preconditioning and postconditioning. Trends Cardiovasc Med 2005; 15:69-75.
30. Schultz J el-J, Hsu AK, Nagase H, Gross GJ: TAN-67, a delta 1-opioid receptor agonist, reduces infarct size via activation of Gi/o proteins and KATP channels. Am J Physiol 1998; 274(3 Pt 2):H909-14.
31. Schultz JE, Hsu AK, Barbieri JT, Li PL, Gross GJ: Pertussis toxin abolishes the cardioprotective effect of ischemic preconditioning in intact rat heart. Am J Physiol 1998; 275(2 Pt 2):H495-H500.
32. Roth DM, Patel HH: Role of caveolae in cardiac protection. Pediatr Cardiol 2011; 32:329-33.
33. Zaugg M, Lucchinetti E, Uecker M, Pasch T, Schaub MC: Anaesthetics and cardiac preconditioning. Part I. Signalling and cytoprotective mechanisms. Br J Anaesth 2003; 91:551-65.
34. Kersten JR, Schmeling TJ, Pagel PS, Gross GJ, Warltier DC: Isoflurane mimics ischemic preconditioning via activation of K(ATP) channels: Reduction of myocardial infarct size with an acute memory phase. Anesthesiology 1997; 87:361-70.
35. Horikawa YT, Patel HH, Tsutsumi YM, Jennings MM, Kidd MW, Hagiwara Y, Ishikawa Y, Insel PA, Roth DM: Caveolin-3 expression and caveolae are required for isoflurane-induced cardiac protection from hypoxia and ischemia/reperfusion injury. J Mol Cell Cardiol 2008; 44:123-30.
36. Minami K, Uezono Y: [The effects of anesthetics on G-proteincoupled receptors]. Masui 2005; 54:118-25.
37. Ludwig LM, Patel HH, Gross GJ, Kersten JR, Pagel PS, Warltier DC: Morphine enhances pharmacological preconditioning byisoflurane: Role of mitochondrial K(ATP) channels and opioid receptors. Anesthesiology 2003; 98:705-11.
38. DeGeorge BR Jr, Gao E, Boucher M, Vinge LE, Martini JS, Raake PW, Chuprun JK, Harris DM, Kim GW, Soltys S, Eckhart AD, Koch WJ: Targeted inhibition of cardiomyocyte Gi signaling enhances susceptibility to apoptotic cell death in response to ischemic stress. Circulation 2008; 117:1378-87.
39. Minshall RD, Tiruppathi C, Vogel SM, Niles WD, Gilchrist A, Hamm HE, Malik AB: Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 2000; 150:1057-70.
40. Murry CE, Richard VJ, Reimer KA, Jennings RB: Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res 1990; 66:913-31.
41. Krajewska WM, Masłowska I: Caveolins: Structure and function in signal transduction. Cell Mol Biol Lett 2004; 9:195-220.
42. Insel PA, Patel HH: Do studies in caveolin-knockouts teach us about physiology and pharmacology or instead, the ways mice compensate for 'lost proteins'? Br J Pharmacol 2007; 150:251-4.
43. Ostrom RS, Bundey RA, Insel PA: Nitric oxide inhibition of adenylyl cyclase type 6 activity is dependent upon lipid rafts and caveolin signaling complexes. J Biol Chem 2004; 279:19846-53.
44. Marinovic J, Bosnjak ZJ, Stadnicka A: Preconditioning by isoflurane induces lasting sensitization of the cardiac sarcolemmal adenosine triphosphate-sensitive potassium channel by a protein kinase C-delta-mediated mechanism. Anesthesiology 2005; 103:540-7.
45. Ludwig LM, Weihrauch D, Kersten JR, Pagel PS, Warltier DC: Protein kinase C translocation and Src protein tyrosine kinase activation mediate isoflurane-induced preconditioning in vivo: Potential downstream targets of mitochondrial adenosine triphosphate-sensitive potassium channels and reactive oxygen species. Anesthesiology 2004; 100:532-9.
46. Krolikowski JG, Bienengraeber M, Weihrauch D, Warltier DC, Kersten JR, Pagel PS: Inhibition of mitochondrial permeability transition enhances isoflurane-induced cardioprotection during early reperfusion: The role of mitochondrial KATP channels. Anesth Analg 2005; 101:1590-6.
47. Schappi JM, Krbanjevic A, Rasenick MM: Tubulin, actin and heterotrimeric G proteins: Coordination of signaling and structure. Biochim Biophys Acta 2014; 1838:674-81.
48. Hu G, Schwartz DE, Shajahan AN, Visintine DJ, Salem MR, Crystal GJ, Albrecht RF, Vogel SM, Minshall RD: Isoflurane, but not sevoflurane, increases transendothelial albumin permeability in the isolated rat lung: Role for enhanced phosphorylation of caveolin-1. Anesthesiology 2006; 104:777-85.