α-SMA-Cre-mediated excision of PDK1 reveals an essential role of PDK1 in regulating morphology of cardiomyocyte and tumor progression in tissue microenvironment

Pathologie Biologie

Volumn 63, Issue 2, 2015, Pages 91-100

  Qian, X J ^a   Li, X L ^b   Xu, X ^a   Wang, X ^a   Feng, Q T ^a   Yang, C J ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Heart failure; Knock out mice; Microenvironment; PDK1; Tumor

Indexed keywords

PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; ACTIN; ALPHA-SMOOTH MUSCLE ACTIN, MOUSE; CRE RECOMBINASE; INTEGRASE; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE (ACETYL-TRANSFERRING) KINASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DISEASE SEVERITY; HEART FUNCTION; HEART MUSCLE CELL; HISTOPATHOLOGY; IN VIVO STUDY; KNOCKOUT MOUSE; LEWIS LUNG CARCINOMA CELL; MEMBRANE PERMEABILITY; METASTASIS; MOUSE; NONHUMAN; PRIMARY TUMOR; PROTEIN FUNCTION; SURVIVAL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL SHAPE; CONGESTIVE CARDIOMYOPATHY; DISEASE COURSE; FEMALE; GENE DELETION; GENE INACTIVATION; GENETICS; MALE; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL CULTURE;

ACTINS; ANIMALS; CARDIOMYOPATHY, DILATED; CELL SHAPE; DISEASE PROGRESSION; FEMALE; GENE DELETION; GENE KNOCKOUT TECHNIQUES; INTEGRASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; NEOPLASM METASTASIS; NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84951568081     PISSN: 03698114     EISSN: 17683114     Source Type: Journal    
DOI: 10.1016/j.patbio.2014.12.004     Document Type: Article

References (46)

1. Vaupel P., Kallinowski F., Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989, 49:6449-6465.
2. Hamada K., Sasaki T., Koni P.A., Natsui M., Kishimoto H., Sasaki J., et al. The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev 2005, 19:2054-2065.
3. Mu Y., Cao G., Zeng Q., Li Y. Transplantation of induced bone marrow mesenchymal stem cells improves the cardiac function of rabbits with dilated cardiomyopathy via upregulation of vascular endothelial growth factor and its receptors. Exp Biol Med (Maywood) 2011, 236:1100-1107.
4. den Heuvel A.F., van V.D.J., der Wall E.E., Blanksma P.K., Siebelink H.M., Vaalburg W.M., et al. Regional myocardial blood flow reserve impairment and metabolic changes suggesting myocardial ischemia in patients with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 2000, 35:19-28.
5. Mazzone M., Dettori D., de Oliveira R.L., Loges S., Schmidt T., Jonckx B., et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009, 136:839-851.
6. Primo L., di B.L., Roca C., Droetto S., Piva R., Schaffhausen B., et al. Essential role of PDK1 in regulating endothelial cell migration. J Cell Biol 2007, 176:1035-1047.
7. Feng Q., Di R., Tao F., Chang Z., Lu S., Fan W., et al. PDK1 regulates vascular remodeling and promotes epithelial-mesenchymal transition in cardiac development. Mol Cell Biol 2010, 30:3711-3721.
8. Chang Z., Zhang Q., Feng Q., Xu J., Teng T., Luan Q., et al. Deletion of Akt1 causes heart defects and abnormal cardiomyocyte proliferation. Dev Biol 2010, 347:384-391.
9. Di R.M., Feng Q.T., Chang Z., Luan Q., Zhang Y.Y., Huang J., et al. PDK1 plays a critical role in regulating cardiac function in mice and human. Chin Med J (Engl) 2010, 123:2358-2363.
10. Blume-Jensen P., Hunter T. Oncogenic kinase signalling. Nature 2001, 411:355-365.
11. Raimondi C., Falasca M. Targeting PDK1 in cancer. Curr Med Chem 2011, 18:2763-2769.
12. Storz P., Toker A. 3'-phosphoinositide-dependent kinase-1 (PDK-1) in PI 3-kinase signaling. Front Biosci 2002, 7:d886-d902.
13. Brazil D.P., Hemmings B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci 2001, 26:657-664.
14. Avruch J., Belham C., Weng Q., Hara K., Yonezawa K. The p70 S6 kinase integrates nutrient and growth signals to control translational capacity. Prog Mol Subcell Biol 2001, 26:115-154.
15. Di R., Wu X., Chang Z., Zhao X., Feng Q., Lu S., et al. S6K inhibition renders cardiac protection against myocardial infarction through PDK1 phosphorylation of Akt. Biochem J 2012, 441:199-207.
16. Newton A.C. Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem J 2003, 370:361-371.
17. Alessi D.R. Discovery of PDK1, one of the missing links in insulin signal transduction. Colworth Medal Lecture. Biochem Soc Trans 2001, 29:1-14.
18. Dong L.Q., Zhang R.B., Langlais P., He H., Clark M., Zhu L., et al. Primary structure, tissue distribution, and expression of mouse phosphoinositide-dependent protein kinase-1, a protein kinase that phosphorylates and activates protein kinase Czeta. J Biol Chem 1999, 274:8117-8122.
19. Lawlor M.A., Mora A., Ashby P.R., Williams M.R., Murray-Tait V., Malone L., et al. Essential role of PDK1 in regulating cell size and development in mice. EMBO J 2002, 21:3728-3738.
20. McManus E.J., Collins B.J., Ashby P.R., Prescott A.R., Murray-Tait V., Armit L.J., et al. The in vivo role of PtdIns(3,4,5)P3 binding to PDK1 PH domain defined by knockin mutation. EMBO J 2004, 23:2071-2082.
21. Pinner S., Sahai E. PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 2008, 10:127-137.
22. Yang L.L., Cheng X., Xiao Y. Generation of smooth muscle cell specific Cre transgenic mice. Bull Acad Mil Med Sci 2005, 3:219-222.
23. Barker N., van E.J.H., Kuipers J., Kujala P., den Born M., v, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
24. Yang Z.Z., Tschopp O., Hemmings-Mieszczak M., Feng J., Brodbeck D., Perentes E., et al. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem 2003, 278:32124-32131.
25. Green T.P., Johnson D.E., Marchessault R.P., Gatto C.W. Transvascular flux and tissue accrual of Evans blue: effects of endotoxin and histamine. J Lab Clin Med 1988, 111:173-183.
26. Peng X., Hassoun P.M., Sammani S., McVerry B.J., et al. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med 2004, 169:1245-1251. [PubMed].
27. Wang L.F., Patel M., Razavi H.M., Weicker S., et al. Role of inducible nitric oxide synthase in pulmonary microvascular protein leak in murine sepsis. Am J Respir Crit Care Med 2002, 165:1634-1639.
28. Green T.P., Johnson D.E., Marchessault R.P., Gatto C.W. Transvascular flux and tissue accrual of Evans blue: effects of endotoxin and histamine. Lab Clin Med 1988, 111:173-183.
29. Mora A., Davies A.M., Bertrand L., Sharif I., Budas G.R., Jovanovic S., et al. Deficiency of PDK1 in cardiac muscle results in heart failure and increased sensitivity to hypoxia. EMBO J 2003, 22:4666-4676.
30. Yang L.L., Cheng X., Xiao Y. Tissue distribution of Cre recombinase in smooth muscle cell specific Cre transgenic mice. Lett Biotechnol 2005, 387-388.
31. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999, 21:70-71.
32. Hinz B., Celetta G., Tomasek J.J., Gabbiani G., Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 2001, 12:2730-2741.
33. Baudino T.A., Carver W., Giles W., Borg T.K. Cardiac fibroblasts: friend or foe. Am J Physiol Heart Circ Physiol 2006, 291:H1015-H1026.
34. Camelliti P., Borg T.K., Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res 2005, 65:40-51.
35. Camelliti P., Green C.R., LeGrice I., Kohl P. Fibroblast network in rabbit sinoatrial node: structural and functional identification of homogeneous and heterogeneous cell coupling. Circ Res 2004, 94:828-835.
36. Sussman M.A., McCulloch A., Borg T.K. Dance band on the Titanic: biomechanical signaling in cardiac hypertrophy. Circ Res 2002, 91:888-898.
37. Gerhardt H., Semb H. Pericytes: gatekeepers in tumour cell metastasis. J Mol Med 2008, 86:135-144.
38. Clement S., Stouffs M., Bettiol E., Kampf S., Krause K.H., Chaponnier C., et al. Expression and function of alpha-smooth muscle actin during embryonic-stem-cell-derived cardiomyocyte differentiation. J Cell Sci 2007, 120:229-238.
39. Adams R.H., Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007, 8:464-478.
40. Coultas L., Chawengsaksophak K., Rossant J. Endothelial cells and VEGF in vascular development. Nature 2005, 438:937-945.
41. Wang J., Chen H., Seth A., McCulloch C.A. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am J Physiol Heart Circ Physiol 2003, 285:H1871-H1881.
42. Leslie K.O., Taatjes D.J., Schwarz J., vonTurkovich M., Low R.B. Cardiac myofibroblasts express alpha smooth muscle actin during right ventricular pressure overload in the rabbit. Am J Pathol 1991, 139:207-216.
43. Souders C.A., Bowers S.L., Baudino T.A. Cardiac fibroblast: the renaissance cell. Circ Res 2009, 105:1164-1176.
44. Joyce J.A. Therapeutic targeting of the tumor microenvironment. Cancer Cell 2005, 7:513-520.
45. van R.J., Song X., van R.W., Cammer M., Chen X., Desmarais V., et al. EGF-induced PIP2 hydrolysis releases and activates cofilin locally in carcinoma cells. J Cell Biol 2007, 179:1247-1259.
46. Humbert M., Montani D., Perros F., Dorfmuller P., Adnot S., Eddahibi S. Endothelial cell dysfunction and cross talk between endothelium and smooth muscle cells in pulmonary arterial hypertension. Vascul Pharmacol 2008, 49:113-118.