Cardiac progenitor cell cycling stimulated by Pim-1 kinase

Circulation Research

Volumn 106, Issue 5, 2010, Pages 891-901

  Cottage, Christopher T ^a   Bailey, Brandi ^a   Fischer, Kimberlee M ^a   Avitable, Daniele ^a   Collins, Brett ^a   Tuck, Savilla ^a   Quijada, Pearl ^a   Gude, Natalie ^a   Alvarez, Roberto ^a   Muraski, John ^a   Sussman, Mark A ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Asymmetric division; Pim 1; Progenitor cells

Indexed keywords

ALPHA ADAPTIN; BROXURIDINE; HISTONE; KI 67 ANTIGEN; PHOSPHOROUS ACID; PROTEIN KINASE PIM 1; MEMBRANE PROTEIN; NERVE PROTEIN; NUMB PROTEIN, MOUSE; PIM1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL COUNT; CELL CYCLE; CELL DIVISION; CELL FATE; CELL POPULATION; CELL PROLIFERATION; CELL REGENERATION; CELL STIMULATION; CELLULAR DISTRIBUTION; CLINICAL ASSESSMENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG EFFECT; GENE OVEREXPRESSION; HEART INFARCTION; MITOSIS; MOUSE; NONHUMAN; ONCOGENE C MYC; POSTNATAL GROWTH; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TRANSGENIC MOUSE; ANIMAL; CELL CULTURE; DISEASE MODEL; ENZYMOLOGY; FEMALE; GENETICS; HEART MUSCLE CELL; MALE; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; REGENERATION; TIME;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ANIMALS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HISTONES; MALE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MUTATION; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-PIM-1; REGENERATION; STEM CELLS; TIME FACTORS;

EID: 77950877955     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.208629     Document Type: Article

References (62)

1. Kajstura J, Urbanek K, Rota M, Bearzi C, Hosoda T, Bolli R, Anversa P, Leri A. Cardiac stem cells and myocardial disease. J Mol Cell Cardiol. 2008;45:505-513.
2. Fransioli J, Bailey B, Gude NA, Cottage CT, Muraski JA, Emmanuel G, Wu W, Alvarez R, Rubio M, Ottolenghi S, Schaefer E, Sussman MA. Evolution of the c-kit positive cell response to pathological challenge in the myocardium. Stem Cells. 2008;26:1315-1324.
3. Chamuleau SA, Vrijsen KR, Rokosh DG, Tang XL, Piek JJ, Bolli R. Cell therapy for ischaemic heart disease: focus on the role of resident cardiac stem cells. Neth Heart J. 2009;17:199-207.
4. Tallini YN, Greene KS, Craven M, Spealman A, Breitbach M, Smith J, Fisher PJ, Steffey M, Hesse M, Doran RM, Woods A, Singh B, Yen A, Fleischmann BK, Kotlikoff MI. c-kit expression identifies cardiovascular precursors in the neonatal heart. Proc Natl Acad Sci U S A. 2009;106:1808-1813.
5. Ikuta K, Weissman IL. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci U S A. 1992;89:1502-1506.
6. Leri A, Kajstura J, Anversa P. Cardiac stem cells and mechanisms of myocardial regeneration. Physiol Rev. 2005;85:1373-1416.
7. Urbanek K, Cesselli D, Rota M, Nascimbene A, De Angelis A, Hosoda T, Bearzi C, Boni A, Bolli R, Kajstura J, Anversa P, Leri A. Stem cell niches in the adult mouse heart. Proc Natl Acad Sci U S A. 2006;103:9226-9231.
8. Linke A, Muller P, Nurzynska D, Casarsa C, Torella D, Nascimbene A, Castaldo C, Cascapera S, Bohm M, Quaini F, Urbanek K, Leri A, Hintze TH, Kajstura J, Anversa P. Stem cells in the dog heart are self-renewing, clonogenic, and multipotent and regenerate infarcted myocardium, improving cardiac function. Proc Natl Acad Sci U S A. 2005;102:8966-8971.
9. Muraski JA, Fischer KM, Wu W, Cottage CT, Quijada P, Mason M, Din S, Gude N, Alvarez R Jr, Rota M, Kajstura J, Wang Z, Schaefer E, Chen X, MacDonnel S, Magnuson N, Houser SR, Anversa P, Sussman MA. Pim-1 kinase antagonizes aspects of myocardial hypertrophy and compensation to pathological pressure overload. Proc Natl Acad Sci U S A. 2008;105:13889-13894.
10. Reiss K, Cheng W, Ferber A, Kajstura J, Li P, Li B, Olivetti G, Homcy CJ, Baserga R, Anversa P. Overexpression of insulin-like growth factor-1 in the heart is coupled with myocyte proliferation in transgenic mice. Proc Natl Acad Sci U S A. 1996;93:8630-8635.
11. Gude N, Muraski J, Rubio M, Kajstura J, Schaefer E, Anversa P, Sussman MA. Akt promotes increased cardiomyocyte cycling and expansion of the cardiac progenitor cell population. Circ Res. 2006;99:381-388.
12. Shiraishi I, Melendez J, Ahn Y, Skavdahl M, Murphy E, Welch S, Schaefer E, Walsh K, Rosenzweig A, Torella D, Nurzynska D, Kajstura J, Leri A, Anversa P, Sussman MA. Nuclear targeting of Akt enhances kinase activity and survival of cardiomyocytes. Circ Res. 2004;94:884-891.
13. Tsujita Y, Muraski J, Shiraishi I, Kato T, Kajstura J, Anversa P, Sussman MA. Nuclear targeting of Akt antagonizes aspects of cardiomyocyte hypertrophy. Proc Natl Acad Sci U S A. 2006;103:11946-11951.
14. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardiomyocytes in vitro and protects against ischemiareperfusion injury in mouse heart. Circulation. 2000;101:660-667.
15. Matsui T, Tao J, del Monte F, Lee KH, Li L, Picard M, Force TL, Franke TF, Hajjar RJ, Rosenzweig A. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation. 2001;104:330-335.
16. Sussman M. "AKT" ing lessons for stem cells: regulation of cardiac myocyte and progenitor cell proliferation. Trends Cardiovasc Med. 2007;17:235-240.
17. Condorelli G, Drusco A, Stassi G, Bellacosa A, Roncarati R, Iaccarino G, Russo MA, Gu Y, Dalton N, Chung C, Latronico MV, Napoli C, Sadoshima J, Croce CM, Ross J Jr. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc Natl Acad Sci U S A. 2002;99:12333-12338.
18. DeBosch B, Sambandam N, Weinheimer C, Courtois M, Muslin AJ. Akt2 regulates cardiac metabolism and cardiomyocyte survival. J Biol Chem. 2006;281:32841-32851.
19. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ. Akt1 is required for physiological cardiac growth. Circulation. 2006;113:2097-2104.
20. Matsui T, Nagoshi T, Hong EG, Luptak I, Hartil K, Li L, Gorovits N, Charron MJ, Kim JK, Tian R, Rosenzweig A. Effects of chronic Akt activation on glucose uptake in the heart. Am J Physiol Endocrinol Metab. 2006;290: E789-E797.
21. Muraski JA, Rota M, Misao Y, Fransioli J, Cottage C, Gude N, Esposito G, Delucchi F, Arcarese M, Alvarez R, Siddiqi S, Emmanuel GN, Wu W, Fischer K, Martindale JJ, Glembotski CC, Leri A, Kajstura J, Magnuson N, Berns A, Beretta RM, Houser SR, Schaefer EM, Anversa P, Sussman MA. Pim-1 regulates cardiomyocyte survival downstream of Akt. Nat Med. 2007;13:1467-1475.
22. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui AL, Kitamura T. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 1999;18:4754-4765.
23. Wang Z, Bhattacharya N, Mixter PF, Wei W, Sedivy J, Magnuson NS. Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase. Biochim Biophys Acta. 2002;1593:45-55.
24. Zhang Y, Wang Z, Li X, Magnuson NS. Pim kinase-dependent inhibition of c-Myc degradation. Oncogene. 2008;27:4809-4819.
25. Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene. 2005;24:2899-2908.
26. Rodriguez-Lopez AM, Xenaki D, Eden TO, Hickman JA, Chresta CM. MDM2 mediated nuclear exclusion of p53 attenuates etoposide-induced apoptosis in neuroblastoma cells. Mol Pharmacol. 2001;59:135-143.
27. Chari NS, Pinaire NL, Thorpe L, Medeiros LJ, Routbort MJ, McDonnell TJ. The p53 tumor suppressor network in cancer and the therapeutic modulation of cell death. Apoptosis. 2009;14:336-347.
28. McDonnell TJ, Chari NS, Cho-Vega JH, Troncoso P, Wang X, Bueso-Ramos CE, Coombes K, Brisbay S, Lopez R, Prendergast G, Logothetis C, Do KA. Biomarker expression patterns that correlate with high grade features in treatment naive, organ-confined prostate cancer. BMC Med Genomics. 2008;1:1.
29. Gude NA, Emmanuel G, Wu W, Cottage CT, Fischer K, Quijada P, Muraski JA, Alvarez R, Rubio M, Schaefer E, Sussman MA. Activation of Notch-mediated protective signaling in the myocardium. Circ Res. 2008;102:1025-1035.
30. Kato T, Muraski J, Chen Y, Tsujita Y, Wall J, Glembotski CC, Schaefer E, Beckerle M, Sussman MA. Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and Akt. J Clin Invest. 2005;115:2716-2730.
31. Leoni LM, Bailey B, Reifert J, Bendall HH, Zeller RW, Corbeil J, Elliott G, Niemeyer CC. Bendamustine (Treanda) displays a distinct pattern of cytotoxicity and unique mechanistic features compared with other alkylating agents. Clin Cancer Res. 2008;14:309-317.
32. Kim KT, Baird K, Ahn JY, Meltzer P, Lilly M, Levis M, Small D. Pim-1 is up-regulated by constitutively activated FLT3 and plays a role in FLT3-mediated cell survival. Blood. 2005;105:1759-1767.
33. Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood. 2005;105:4477-4483.
34. Aksoy I, Sakabedoyan C, Bourillot PY, Malashicheva AB, Mancip J, Knoblauch K, Afanassieff M, Savatier P. Self-renewal of murine embryonic stem cells is supported by the serine/threonine kinases Pim-1 and Pim-3. Stem Cells. 2007;25:2996-3004.
35. Bailey B, Izarra A, Alvarez R, Fischer KM, Cottage CT, Quijada P, Diez-Juan A, Sussman MA. Cardiac stem cell genetic engineering using the alphaMHC promoter. Regen Med. 2009;4:823-833.
36. Bhattacharya N, Wang Z, Davitt C, McKenzie IF, Xing PX, Magnuson NS. Pim-1 associates with protein complexes necessary for mitosis. Chromosoma. 2002;111:80-95.
37. Wu JC. Molecular imaging: antidote to cardiac stem cell controversy. J Am Coll Cardiol. 2008;52:1661-1664.
38. Liu J, Sluijter JP, Goumans MJ, Smits AM, van der Spoel T, Nathoe H, Doevendans PA. Cell therapy for myocardial regeneration. Curr Mol Med. 2009;9:287-298.
39. Gnecchi M, He H, Melo LG, Noiseaux N, Morello F, de Boer RA, Zhang L, Pratt RE, Dzau VJ, Ingwall JS. Early beneficial effects of bone marrow-derived mesenchymal stem cells overexpressing Akt on cardiac metabolism after myocardial infarction. Stem Cells. 2009;27:971-979.
40. Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103:1204-1219.
41. Gnecchi M, He H, Noiseux N, Liang OD, Zhang L, Morello F, Mu H, Melo LG, Pratt RE, Ingwall JS, Dzau VJ. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J. 2006;20:661-669.
42. Sun QY, Schatten H. Role of NuMA in vertebrate cells: review of an intriguing multifunctional protein. Front Biosci. 2006;11:1137-1146.
43. Zhang Y, Wang Z, Magnuson NS. Pim-1 kinase-dependent phosphorylation of p21Cip1/WAF1 regulates its stability and cellular localization in H1299 cells. Mol Cancer Res. 2007;5:909-922.
44. Stewart ZA, Leach SD, Pietenpol JA. p21 (Waf1/Cip1) inhibition of cyclin E/Cdk2 activity prevents endoreduplication after mitotic spindle disruption. Mol Cell Biol. 1999;19:205-215.
45. Liang H, Hittelman W, Nagarajan L. Ubiquitous expression and cell cycle regulation of the protein kinase PIM-1. Arch Biochem Biophys. 1996;330:259-265.
46. Limana F, Urbanek K, Chimenti S, Quaini F, Leri A, Kajstura J, Nadal-Ginard B, Izumo S, Anversa P. bcl-2 overexpression promotes myocyte proliferation. Proc Natl Acad Sci U S A. 2002;99:6257-6262.
47. Nebigil CG, Jaffre F, Messaddeq N, Hickel P, Monassier L, Launay JM, Maroteaux L. Overexpression of the serotonin 5-HT2B receptor in heart leads to abnormal mitochondrial function and cardiac hypertrophy. Circulation. 2003;107:3223-3229.
48. Karpanen T, Bry M, Ollila HM, Seppanen-Laakso T, Liimatta E, Leskinen H, Kivela R, Helkamaa T, Merentie M, Jeltsch M, Paavonen K, Andersson LC, Mervaala E, Hassinen IE, Yla-Herttuala S, Oresic M, Alitalo K. Overexpression of vascular endothelial growth factor-B in mouse heart alters cardiac lipid metabolism and induces myocardial hypertrophy. Circ Res. 2008;103:1018-1026.
49. Urayama K, Guilini C, Messaddeq N, Hu K, Steenman M, Kurose H, Ert G, Nebigil CG. The prokineticin receptor-1 (GPR73) promotes cardiomyocyte survival and angiogenesis. FASEB J. 2007;21:2980-2993.
50. Ponten A, Li X, Thoren P, Aase K, Sjoblom T, Ostman A, Eriksson U. Transgenic overexpression of platelet-derived growth factor-C in the mouse heart induces cardiac fibrosis, hypertrophy, and dilated cardiomyopathy. Am J Pathol. 2003;163:673-682.
51. Pasumarthi KB, Nakajima H, Nakajima HO, Soonpaa MH, Field LJ. Targeted expression of cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ Res. 2005;96:110-118.
52. Shioi T, McMullen JR, Kang PM, Douglas PS, Obata T, Franke TF, Cantley LC, Izumo S. Akt/protein kinase B promotes organ growth in transgenic mice. Mol Cell Biol. 2002;22:2799-2809.
53. Schiekofer S, Shiojima I, Sato K, Galasso G, Oshima Y, Walsh K. Microarray analysis of Akt1 activation in transgenic mouse hearts reveals transcript expression profiles associated with compensatory hypertrophy and failure. Physiol Genomics. 2006;27:156-170.
54. Matsui T, Li L, Wu JC, Cook SA, Nagoshi T, Picard MH, Liao R, Rosenzweig A. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J Biol Chem. 2002;277:22896-22901.
55. Petersen PH, Tang H, Zou K, Zhong W. The enigma of the numb-Notch relationship during mammalian embryogenesis. Dev Neurosci. 2006;28:156-168.
56. Zhong W, Chia W. Neurogenesis and asymmetric cell division. Curr Opin Neurobiol. 2008;18:4-11.
57. Yu LZ, Xiong B, Gao WX, Wang CM, Zhong ZS, Huo LJ, Wang Q, Hou Y, Liu K, Liu XJ, Schatten H, Chen DY, Sun QY. MEK1/2 regulates microtubule organization, spindle pole tethering and asymmetric division during mouse oocyte meiotic maturation. Cell Cycle. 2007;6:330-338.
58. Yang YM, Chang JW. Current status and issues in cancer stem cell study. Cancer Invest. 2008;26:741-755.
59. Fabian A, Barok M, Vereb G, Szollosi J. Die hard: are cancer stem cells the Bruce Willises of tumor biology? Cytometry A. 2009;75:67-74.
60. Jackson T, Allard MF, Sreenan CM, Doss LK, Bishop SP, Swain JL. The c-myc proto-oncogene regulates cardiac development in transgenic mice. Mol Cell Biol. 1990;10:3709-3716.
61. Jackson T, Allard MF, Sreenan CM, Doss LK, Bishop SP, Swain JL. Transgenic animals as a tool for studying the effect of the c-myc proto-oncogene on cardiac development. Mol Cell Biochem. 1991;104:15-19.
62. Reiss K, Capasso JM, Huang HE, Meggs LG, Li P, Anversa P. ANG II receptors, c-myc, and c-jun in myocytes after myocardial infarction and ventricular failure. Am J Physiol. 1993;264: H760-H769. (Pubitemid 23109866)