AMPK attenuates microtubule proliferation in cardiac hypertrophy

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 5, 2013, Pages

  Fassett, John T ^a   Hu, Xinli ^a   Xu, Xin ^a   Lu, Zhongbing ^a   Zhang, Ping ^a   Chen, Yingjie ^a   Bache, Robert J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

AMP activated protein kinase; Cytoskeleton; Hypertrophy; Microtubule; Microtubule associated protein 4

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ADENYLATE KINASE; MICROTUBULE ASSOCIATED PROTEIN 4; PHENYLEPHRINE; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL EXPANSION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; GROWTH; GROWTH REGULATION; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; INTERMEDIATE FILAMENT; MICROTUBULE; MOUSE; MYOFILAMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; CARDIOMEGALY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; TUBULIN; VENTRICULAR PRESSURE;

EID: 84874641762     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00935.2011     Document Type: Article

References (46)

1. Bannai H, Inoue T, Nakayama T, Hattori M, Mikoshiba K. Kinesin dependent, rapid, bi-directional transport of ER sub-compartment in dendrites of hippocampal neurons. J Cell Sci 117: 163-175, 2004.
2. Cheng G, Qiao F, Gallien TN, Kuppuswamy D, Cooper G. Inhibition of β-adrenergic receptor trafficking in adult cardiocytes by MAP4 decoration of microtubules. Am J Physiol Heart Circ Physiol 288: H1193-H1202, 2005.
3. Cheng G, Takahashi M, Shunmugavel A, Wallenborn JG, DePaoli-Roach AA, Gergs U, Neumann J, Kuppuswamy D, Menick DR, Cooper G. Basis for MAP4 dephosphorylation-related microtubule network densification in pressure overload cardiac hypertrophy. J Biol Chem 285: 38125-38140, 2010.
4. Chinnakkannu P, Samanna V, Cheng G, Ablonczy Z, Baicu CF, Bethard JR, Menick DR, Kuppuswamy D, Cooper G. Site-specific microtubule-associated protein 4 dephosphorylation causes microtubule network densification in pressure overload cardiac hypertrophy. J Biol Chem 285: 21837-21848, 2010.
5. Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E. MARK, a novel family of protein kinases that phosphorylate microtubuleassociated proteins and trigger microtubule disruption. Cell 89: 297-308, 1997.
6. Ebneth A, Drewes G, Mandelkow EM, Mandelkow E. Phosphorylation of MAP2c and MAP4 by MARK kinases leads to the destabilization of microtubules in cells. Cell Motil Cytoskeleton 44: 209-224, 1999.
7. Fassett JT, Xu X, Hu X, Zhu G, French J, Chen Y, Bache RJ. Adenosine regulation of microtubule dynamics in cardiac hypertrophy. Am J Physiol Heart Circ Physiol 297: H523-H532, 2009.
8. Foretz M, Ancellin N, Andreelli F, Saintillan Y, Grondin P, Kahn A, Thorens B, Vaulont S, Viollet B. Short-term overexpression of a constitutively active form of AMP-activated protein kinase in the liver leads to mild hypoglycemia and fatty liver. Diabetes 54: 1331-1339, 2005.
9. Frederick RL, Shaw JM. Moving mitochondria: establishing distribution of an essential organelle. Traffic 8: 1668-1675, 2007.
10. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30: 214-226, 2008.
11. Hu P, Zhang D, Swenson L, Chakrabarti G, Abel ED, Litwin SE. Minimally invasive aortic banding in mice: effects of altered cardiomyocyte insulin signaling during pressure overload. Am J Physiol Heart Circ Physiol 285: H1261-H1269, 2003.
12. Illenberger S, Drewes G, Trinczek B, Biernat J, Meyer HE, Olmsted JB, Mandelkow EM, Mandelkow E. Phosphorylation of microtubuleassociated proteins MAP2 and MAP4 by the protein kinase p110mark. Phosphorylation sites and regulation of microtubule dynamics. J Biol Chem 271: 10834-10843, 1996.
13. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590, 2003.
14. 2+ spark rate. Circ Res 104: 787-795, 2009.
15. Koide M, Hamawaki M, Narishige T, Sato H, Nemoto S, DeFreyte G, Zile MR, Cooper G, Carabello BA. Microtubule depolymerization normalizes in vivo myocardial contractile function in dogs with pressureoverload left ventricular hypertrophy. Circulation 102: 1045-1052, 2000.
16. Lauf U, Giepmans BN, Lopez P, Braconnot S, Chen SC, Falk MM. Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc Natl Acad Sci USA 99: 10446-10451, 2002.
17. Mandelkow EM, Thies E, Trinczek B, Biernat J, Mandelkow E. MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J Cell Biol 167: 99-110, 2004.
18. Marx A, Nugoor C, Panneerselvam S, Mandelkow E. Structure and function of polarity-inducing kinase family MARK/Par-1 within the branch of AMPK/Snf1-related kinases. FASEB J 24: 1637-1648, 2010.
19. Matsushima K, Tokuraku K, Hasan MR, Kotani S. Microtubuleassociated protein 4 binds to actin filaments and modulates their properties. J Biochem 151: 99-108, 2012.
20. Nakano A, Kato H, Watanabe T, Min KD, Yamazaki S, Asano Y, Seguchi O, Higo S, Shintani Y, Asanuma H, Asakura M, Minamino T, Kaibuchi K, Mochizuki N, Kitakaze M, Takashima S. AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat Cell Biol 12: 583-590.
21. Nakano A, Kato H, Watanabe T, Min KD, Yamazaki S, Asano Y, Seguchi O, Higo S, Shintani Y, Asanuma H, Asakura M, Minamino T, Kaibuchi K, Mochizuki N, Kitakaze M, Takashima S. AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat Cell Biol 12: 583-590, 2010.
22. Perhonen M, Sharp WW, Russell B. Microtubules are needed for dispersal of alpha-myosin heavy chain mRNA in rat neonatal cardiac myocytes. J Mol Cell Cardiol 30: 1713-1722, 1998.
23. Prosser BL, Ward CW, Lederer WJ. X-ROS signaling: rapid mechanochemo transduction in heart. Science 333: 1440-1445, 2011.
24. Sato H, Nagai T, Kuppuswamy D, Narishige T, Koide M, Menick DR, Cooper G. Microtubule stabilization in pressure overload cardiac hypertrophy. J Cell Biol 139: 963-973, 1997.
25. Scholz D, Baicu CF, Tuxworth WJ, Xu L, Kasiganesan H, Menick DR, Cooper G. Microtubule-dependent distribution of mRNA in adult cardiocytes. Am J Physiol Heart Circ Physiol 294: H1135-H1144, 2008.
26. Scholz D, McDermott P, Garnovskaya M, Gallien TN, Huettelmaier S, DeRienzo C, Cooper G. Microtubule-associated protein-4 (MAP-4) inhibits microtubule-dependent distribution of mRNA in isolated neonatal cardiocytes. Cardiovasc Res 71: 506-516, 2006.
27. Scholz D, McDermott P, Garnovskaya M, Gallien TN, Huettelmaier S, DeRienzo C, and Cooper GT. Microtubule-associated protein-4 (MAP-4) inhibits microtubule-dependent distribution of mRNA in isolated neonatal cardiocytes. Cardiovasc Res 71: 506-516, 2006.
28. Shaw RJ. LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol (Oxf) 196: 65-80, 2009.
29. Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN, Jan LY. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 128: 547-560, 2007.
30. Shende P, Plaisance I, Morandi C, Pellieux C, Berthonneche C, Zorzato F, Krishnan J, Lerch R, Hall MN, Ruegg MA, Pedrazzini T, Brink M. Cardiac raptor ablation impairs adaptive hypertrophy, alters metabolic gene expression, and causes heart failure in mice. Circulation 123: 1073-1082, 2011.
31. Shioi T, McMullen JR, Tarnavski O, Converso K, Sherwood MC, Manning WJ, Izumo S. Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circulation 107: 1664-1670, 2003.
32. Smyth JW, Hong TT, Gao D, Vogan JM, Jensen BC, Fong TS, Simpson PC, Stainier DY, Chi NC, Shaw RM. Limited forward trafficking of connexin 43 reduces cell-cell coupling in stressed human and mouse myocardium. J Clin Invest 120: 266-279, 2010.
33. Song X, Kusakari Y, Xiao CY, Kinsella SD, Rosenberg MA, Scherrer-Crosbie M, Hara K, Rosenzweig A, Matsui T. mTOR attenuates the inflammatory response in cardiomyocytes and prevents cardiac dysfunction in pathological hypertrophy. Am J Physiol Cell Physiol 299: C1256-C1266, 2010.
34. Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, House CM, Fernandez CS, Cox T, Witters LA, Kemp BE. Mammalian AMP-activated protein kinase subfamily. J Biol Chem 271: 611-614, 1996.
35. Tagawa H, Koide M, Sato H, Zile MR, Carabello BA, Cooper G. Cytoskeletal role in the transition from compensated to decompensated hypertrophy during adult canine left ventricular pressure overloading. Circ Res 82: 751-761, 1998.
36. Tagawa H, Wang N, Narishige T, Ingber DE, Zile MR, Cooper G. Cytoskeletal mechanics in pressure-overload cardiac hypertrophy. Circ Res 80: 281-289, 1997.
37. Takahashi M, Shiraishi H, Ishibashi Y, Blade KL, McDermott PJ, Menick DR, Kuppuswamy D, Cooper G. Phenotypic consequences of beta1-tubulin expression and MAP4 decoration of microtubules in adult cardiocytes. Am J Physiol Heart Circ Physiol 285: H2072-H2083, 2003.
38. Terasaki M, Chen LB, Fujiwara K. Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 103: 1557-1568, 1986.
39. Thornton C, Bright NJ, Sastre M, Muckett PJ, Carling D. AMPactivated protein kinase (AMPK) is a tau kinase, activated in response to amyloid beta-peptide exposure. Biochem J 434: 503-512, 2011.
40. Thyberg J, Moskalewski S. Role of microtubules in the organization of the Golgi complex. Exp Cell Res 246: 263-279, 1999.
41. Tsutsui H, Ishihara K, Cooper G. Cytoskeletal role in the contractile dysfunction of hypertrophied myocardium. Science 260: 682-687, 1993.
42. Welte MA. Bidirectional transport along microtubules. Curr Biol 14: R525-R537, 2004.
43. Yaffe MP, Harata D, Verde F, Eddison M, Toda T, Nurse P. Microtubules mediate mitochondrial distribution in fission yeast. Proc Natl Acad Sci USA 93: 11664-11668, 1996.
44. Yi M, Weaver D, Hajnoczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167: 661-672, 2004.
45. Zhang D, Contu R, Latronico MV, Zhang J, Rizzi R, Catalucci D, Miyamoto S, Huang K, Ceci M, Gu Y, Dalton ND, Peterson KL, Guan KL, Brown JH, Chen J, Sonenberg N, Condorelli G. MTORC1 regulates cardiac function and myocyte survival through 4E-BP1 inhibition in mice. J Clin Invest 120: 2805-2816, 2010.
46. Zhang P, Hu X, Xu X, Fassett J, Zhu G, Viollet B, Xu W, Wiczer B, Bernlohr DA, Bache RJ, Chen Y. AMP activated protein kinase-alpha2 deficiency exacerbates pressure-overload-induced left ventricular hypertrophy and dysfunction in mice. Hypertension 52: 918-924, 2008.