Nitric oxide-cyclic GMP signaling in stem cell differentiation

Free Radical Biology and Medicine

Volumn 51, Issue 12, 2011, Pages 2150-2157

  Mujoo, Kalpana ^a   Krumenacker, Joshua S ^b   Murad, Ferid ^c  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b INDIANA UNIVERSITY   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Cyclic GMP; Differentiation; Free radicals; Nitric oxide; Stem cells

Indexed keywords

CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANYLATE CYCLASE; NITRIC OXIDE; SOLUABLE GUANYLATE CYCLASE; UNCLASSIFIED DRUG;

ALLOSTERISM; CELL DIFFERENTIATION; EMBRYO DEVELOPMENT; GENETIC MANIPULATION; HEART MUSCLE CELL; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CYCLIC GMP; HUMANS; NITRIC OXIDE; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 81855167110     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.09.037     Document Type: Review

References (147)

1. J.S. Beckman, and W.H. Koppenol Nitric oxide, superoxide and peroxynitrite: the good, the bad and the ugly Am. J. Physiol. 271 1996 C1424 C1437
2. N.S. Bryan, K. Bian, and F. Murad Discovery of nitric oxide signaling pathways and targets for drug development Front. Biosci. 14 2009 1 18
3. F. Murad Shattuck lecture: nitric oxide and cyclic GMP in cell signaling and drug development N. Engl. J. Med. 355 2006 2003 2011 (Pubitemid 44708019)
4. S. Moncada, R.M.J. Palmer, and J. Higgs Nitric oxide; physiology, patho-physiology and pharmacology Pharmacol. Rev. 43 1991 109 142
5. H. Xia, and D.S. Bredt Cloned and expressed nitric oxide synthase proteins Methods Enzymol. 268 1996 427 436 (Pubitemid 26286385)
6. K.A. White, and M.A. Marletta Nitric oxide synthase is a cytochrome-P450 type heme protein Biochemistry 31 1992 6627 6631
7. H.M. Abu-Soud, L.L. Yoho, and D.J. Stuehr Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer Proc. Natl. Acad. Sci. U. S. A. 90 1993 10769 10772 (Pubitemid 23347124)
8. Q. Liu, and S.S. Gross Binding sites of nitric oxide synthases Methods Enzymol. 268 1996 311 324 (Pubitemid 26286373)
9. J.S. Krumenacker, K.A. Hanafy, and F. Murad Regulation of nitric oxide and soluble guanylyl cyclase Brain Res. Bull. 62 2004 505 515 (Pubitemid 38253036)
10. M. Russwurm, S. Behrends, C. Harteneck, and D. Koesling Functional properties of a naturally occurring isoform of soluble guanylyl cyclase Biochem. J. 355 1998 125 130 (Pubitemid 28477058)
11. J. Budworth, S. Meillerais, I. Charles, and K. Powell Tissue distribution of the human guanylate cyclases Biochem. Biophys. Res. Commun. 263 1999 696 701 (Pubitemid 29490689)
12. E. Mergia, M. Russwurm, G. Zoidl, and D. Kosling Major occurrence of the new alpha2beta1 isoform of NO-sensitive guanylyl cyclase in brain Cell. Signal. 15 2003 189 195 (Pubitemid 35449122)
13. K.A. Lucas, G.M. Pitari, S. Kazerounian, I. Ruiz-Stewart, J. Park, S. Schulz, K.P. Chepenik, and S.A. Waldman Guanylyl cyclases and signaling by cyclic GMP Pharmacol. Rev. 52 2000 375 414
14. M. Biel, M. Seeliger, A. Pfeifer, K. Kohler, A. Gerstner, A. Ludwig, G. Jaissle, S. Fauser, E. Zrenner, and F. Hofmann Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3 Proc. Natl. Acad. Sci. U. S. A. 96 1999 7553 7557 (Pubitemid 29299700)
15. M. Boolell, M.J. Allen, S.A. Ballard, S. Gepi-Attee, G.J. Muirhead, A.M. Naylor, I.H. Osterloh, and C. Gingell Sildenafil: an orally active type 5 cyclic GMP-specific phosphodiesterase inhibitor for the treatment of penile erectile dysfunction Int. J. Impot. Res. 8 1996 47 52
16. 1 subunits of the mammalian soluble guanylyl cyclase genes Proc. Natl. Acad. Sci. U. S. A. 97 2000 10878 10883
17. J.S. Krumenacker, S.M. Hyder, and F. Murad Estradiol rapidly inhibits soluble guanylyl cyclase expression in rat uterus Proc. Natl. Acad. Sci. U. S. A. 98 2001 717 722 (Pubitemid 32105109)
18. P. Humbert, F. Niroomand, B. Mayer, D. Koesling, K.D. Hinsch, H. Gausepohl, R. Frank, G. Schulz, and E. Bohme Purification of soluble guanylyl cyclases from bovine lung by a new immunoaffinity chromatographic method Eur. J. Biochem./FEBS 190 1990 273 278 (Pubitemid 20201512)
19. Y.C. Lee, E. Martin, and F. Murad Human recombinant soluble guanylyl cyclase: expression, purification and regulation Proc. Natl. Acad. Sci. U. S. A. 97 2000 10763 10768
20. A. Pyriochou, and A. Papapetropoulos Soluble guanylyl cyclase; more secrets revealed Cell. Signal. 17 2005 407 413 (Pubitemid 39643059)
21. A. Papapetropoulos, C.Y. Go, F. Murad, and J.D. Catravas Mechanisms of tolerance to sodium nitroprusside in rat cultured aortic smooth muscle cells Br. J. Pharmacol. 117 1996 147 155 (Pubitemid 26030264)
22. S. Klöss, R. Srivastava, and A. Mülsch Down-regulation of soluble guanylyl cyclase expression by cyclic AMP is mediated by mRNA-stabilizing protein HuR Mol. Pharmacol. 65 2004 1440 1451 (Pubitemid 38668302)
23. A. Papapetropoulos, N. Marczin, G. Mora, A. Milici, F. Murad, and J.D. Catravas Regulation of vascular smooth muscle soluble guanylate cyclase activity, mRNA, and protein levels by cAMP-elevating agents Hypertension 26 1995 696 704
24. A. Papapetropoulos, G. Abou-Mohamed, N. Marczin, F. Murad, R.W. Caldwell, and J.D. Catravas Downregulation of nitrovasodilator-induced cyclic GMP accumulation in cells exposed to endotoxin or interleukin-1 beta Br. J. Pharmacol. 118 1996 1359 1366 (Pubitemid 26248784)
25. S. Behrends, C. Harteneck, G. Schultz, and D. Koesling A variant of the alpha 2 subunit of soluble guanylyl cyclase contains an insert homologous to a region within adenylyl cyclases and functions as a dominant negative protein J. Biol. Chem. 270 1995 21109 21113
26. S. Behrends, and K. Vehse The beta(2) subunit of soluble guanylyl cyclase contains a human-specific frameshift and is expressed in gastric carcinoma Biochem. Biophys. Res. Commun. 271 2000 64 69 (Pubitemid 30444857)
27. V. Chhajlani, P.A. Frändberg, J. Ahlner, K.L. Axelsson, and J.E. Wikberg Heterogeneity in human soluble guanylate cyclase due to alternative splicing FEBS Lett. 290 1991 157 158
28. H. Okamoto Molecular cloning of a novel variant of the rat soluble guanylate cyclase beta 2 subunit Int. J. Biochem. Cell Biol. 36 2004 472 480 (Pubitemid 37542445)
29. I.G. Sharina, F. Jelen, E.P. Bogatenkova, A. Thomas, E. Martin, and F. Murad Alpha1 soluble guanylyl cyclase (sGC) splice forms as potential regulators of human sGC activity J. Biol. Chem. 283 2008 15104 15113
30. O.V. Evgenov, P. Pacher, P.M. Schmidt, G. Hasko, H.H.H.W. Schmidt, and J.-P. Stasch NO-independent stimulators and activators of soluble guanylyl cyclase: discovery and therapeutic potential Nat. Rev. 5 2006 755 768 (Pubitemid 44323702)
31. E. Martin, Y.C. Lee, and F. Murad YC-1 activation of human soluble guanylyl cyclase has both heme-dependent and heme-independent components Proc. Natl. Acad. Sci. U. S. A. 98 2001 12938 12942 (Pubitemid 33051298)
32. A. Aszódi, A. Pfeifer, M. Ahmad, M. Glauner, X.-H. Zhou, L. Ny, K.E. Andersson, B. Kehrel, S. Offermanns, and R. Fässler The vasodilator-stimulated phosphoprotein (VASP) is involved in cGMP- and cAMP-mediated inhibition of agonist-induced platelet aggregation, but is dispensable for smooth muscle function EMBO J. 18 1999 37 48 (Pubitemid 29005021)
33. S. Endo, M. Suzuki, M. Sumi, A.C. Nairn, R. Morita, K. Yamakawa, P. Greengard, and M. Ito Molecular identification of human G-substrate, a possible downstream component of the cGMP dependent protein kinase cascade in cerebellar Purkinje cells Proc. Natl. Acad. Sci. U. S. A. 96 1999 2467 2472 (Pubitemid 29117939)
34. P. Komalavilas, and T.M. Lincoln Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic GMP-dependent protein kinase J. Biol. Chem. 269 1994 8701 8707 (Pubitemid 24209175)
35. K.B. Pryzwansky, T.A. Wyatt, and T.M. Lincoln Cyclic guanosine monophosphate-dependent protein kinase is targeted to intermediate filaments and phosphorylates vimentin in A23187-stimulated human neutrophils Blood 85 1995 222 230
36. 2+ pump of bovine pulmonary artery Cell Calcium 11 1990 261 268 (Pubitemid 20134356)
37. H.K. Surks, N. Mochizuki, Y. Kasai, S.P. Georgescu, K.M. Tang, M. Ito, T.M. Lincoln, and M.E. Mendelsohn Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase I alpha Science 286 1999 1583 1587
38. T. Jarchau, C. Häusler, T. Markert, D. Pöhler, J. Vanderkerckhove, H.R. De Jonge, S.M. Lohmann, and U. Walter Cloning, expression, and in situ localization of rat intestinal cGMP-dependent protein kinase II Proc. Natl. Acad. Sci. U. S. A. 91 1994 9426 9430
39. S.M. Lohmann, A.B. Vaandrager, A. Smolenski, U. Walter, and H.R. De Jonge Distinct and specific functions of cGMP-dependent protein kinases Trends Biochem. Sci. 22 1997 307 312 (Pubitemid 27327088)
40. S. Orstavik, R. Solberg, K. Taskén, M. Nordahl, M.R. Altherr, V. Hansson, T. Jahnsen, and M. Sandberg Molecular cloning, cDNA structure, and chromosomal localization of the human type II cGMP-dependent protein kinase Biochem. Biophys. Res. Commun. 220 1996 759 765 (Pubitemid 26198584)
41. N. Tamura, H. Itoh, Y. Ogawa, O. Nakagawa, M. Harada, T.H. Chun, S. Suga, T. Yoshimasa, and K. Nakao cDNA cloning and gene expression of human type Ialpha cGMP-dependent protein kinase Hypertension 27 1996 552 557 (Pubitemid 26086223)
42. M.D. Uhler Cloning and expression of a novel cyclic GMP-dependent protein kinase from mouse brain J. Biol. Chem. 268 1993 13586 13591 (Pubitemid 23307789)
43. E.J. Tsai, and D.A. Kass Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics Pharmacol. Ther. 122 2009 216 238
44. C. Lugnier, T. Keravis, and A. Eckly-Michel Cross talk between NO and cyclic nucleotide phosphodiesterases in the modulation of signal transduction in blood vessel J. Physiol. Pharmacol. 50 1999 639 652 (Pubitemid 30022142)
45. D.H. Maurice Cyclic nucleotide phosphodiesterase-mediated integration of cGMP and cAMP signaling in cells of the cardiovascular system Front. Biosci. 10 2005 1221 1228
46. S.J. Netherton, and D.H. Maurice Vascular endothelial cell cyclic nucleotide phosphodiesterases and regulated cell migration: implications in angiogenesis Mol. Pharmacol. 67 2005 263 272 (Pubitemid 40069987)
47. O. Pauvert, D. Salvail, E. Rousseau, C. Lugnier, R. Marthan, and J.P. Savineau Characterisation of cyclic nucleotide phosphodiesterase isoforms in the media layer of the main pulmonary artery Biochem. Pharmacol. 63 2002 1763 1772 (Pubitemid 34458014)
48. P.G. Phillips, L. Long, M.R. Wilkins, and N.W. Morrell cAMP phosphodiesterase inhibitors potentiate effects of prostacyclin analogs in hypoxic pulmonary vascular remodeling Am. J. Physiol. Lung Cell. Mol. Physiol. 288 2005 L103 L115
49. K. Sadhu, K. Hensley, V.A. Florio, and S.L. Wolda Differential expression of the cyclic GMP-stimulated phosphodiesterase PDE2A in human venous and capillary endothelial cells J. Histochem. Cytochem. 47 1999 895 906
50. W.J. Thompson, T. Ashikaga, J.J. Kelly, L. Liu, B. Zhu, L. Vemavarapu, and S.J. Strada Regulation of cyclic AMP in rat pulmonary micro vascular endothelial cells by rolipram-sensitive cyclic AMP phosphodiesterase (PDE4) Biochem. Pharmacol. 63 2002 797 807 (Pubitemid 34457713)
51. E. Takimoto, D. Belardi, C.G. Tocchetti, S. Vahebi, G. Cormaci, E.A. Ketner, A.L. Moens, H.C. Champion, and D.A. Kass Compartmentalization of cardiac beta-adrenergic inotropy modulation by phosphodiesterase type 5 Circulation 115 2007 2159 2167 (Pubitemid 46659068)
52. M. Zhang, N. Koitabashi, T. Nagayama, R. Rambaran, N. Feng, E. Takimoto, T. Koenke, B. O'Rourke, H.C. Champion, M.T. Crow, and D.A. Kass Expression, activity, and pro-hypertrophic effects of PDE5A in cardiac myocytes Cell. Signal. 20 2008 2231 2236
53. S. Tranguch, and Y. Huet-Hudson Decreased viability of nitric oxide synthase double knockout mice Mol. Reprod. Dev. 65 2003 175 179 (Pubitemid 36539207)
54. T.C. Lee, Y.D. Zhao, D.W. Courtman, and D.J. Stewart Abnormal aortic valve development in mice lacking endothelial nitric oxide synthase Circulation 101 2000 2345 2348 (Pubitemid 30329122)
55. Q. Feng, W. Song, X. Lu, J.A. Hamilton, M. Lei, T. Peng, and S.P. Yee Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase Circulation 106 2002 873 879
56. M. Tsutsui, H. Shimokawa, T. Morishita, Y. Nakashima, and N. Yanagihara Development of genetically engineered mice lacking all three nitric oxide synthases J. Pharmacol. Sci. 102 2006 147 154 (Pubitemid 44690971)
57. H.-W. Chen, W.-S. Jiang, and C.-R. Tzeng Nitric oxide as a regulator in preimplantation embryo development and apoptosis Fertil. Steril. 75 2001 1163 1171 (Pubitemid 32522615)
58. S. Nimmegeers, P. Sips, E. Buys, P. Brouckaert, and J. Van de Voorde Functional role of the soluble guanylyl cyclase alpha(I) subunit in vascular smooth muscle relaxation Cardiovasc. Res. 76 2007 149 159 (Pubitemid 47362046)
59. A. Friebe, E. Mergia, O. Dangel, A. Lange, and D. Koesling Fatal gastrointestinal obstruction and hypertension in mice lacking nitric oxide-sensitive guanylyl cyclase Proc. Natl. Acad. Sci. U. S. A. 104 2007 7699 7704 (Pubitemid 47185969)
60. J. Schlossmann, R. Feil, and F. Hofmann Insights into cGMP signalling derived from cGMP kinase knockout mice Front. Biosci. 10 2005 1279 1289
61. F. Hoffman, R. Feil, T. Kleppisch, and J. Schlossmann Function of cGMP dependent protein kinases as revealed by gene deletion Physiol. Rev. 86 2006 1 23
62. V. Volarevic, B. Ljujic, P. Stojkovic, A. Lukic, N. Arsenijevic, and M. Stojkovic Human stem cell research and regenerative medicine-present and future Br. Med. Bull. 99 2011 155 168
63. A.C. Brignier, and A.M. Gewirtz Embryonic and adult stem cell therapy J. Allergy Clin. Immunol. 125 2010 S336 S344
64. C. Dambrot, R. Passier, D. Atsma, and C.L. Mummery Cardiomyocyte differentiation of pluripotent stem cells and their use as cardiac disease models Biochem. J. 434 2011 25 35
65. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147 (Pubitemid 28516247)
66. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 633 676
67. K. Okita, T. Ischisaka, and S. Yamanaka Generation of germline-competent induced pluripotent stem cells Nature 448 2007 313 317 (Pubitemid 47080336)
68. N. Maherali, R. Sridharan, W. Xie, J. Utikal, S. Eminli, K. Arnold, M. Stadtfeld, R. Yachechko, J. Tchieu, R. Jaenisch, K. Plath, and K. Hochedlinger Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution Cell Stem Cell 7 2007 55 70
69. M. Wernig, A. Meissner, R. Foreman, T. Brambrink, M. Ku, K. Hochedlinger, B.E. Bernstein, and R. Jaenisch In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state Nature 448 2007 318 324 (Pubitemid 47080337)
70. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, K. Tomoda, and S. Yamanaka Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872 (Pubitemid 350138099)
71. J. Yu, M.A. Vodyanik, K. Smuga-Otto, J. Antosiewicz-Bourget, J.L. Frane, S. Tian, J. Nie, G.A. Jonsdottir, V. Ruotti, R. Stewart, I.I. Slukvin, and J.A. Thomson Induced pluripotent stem cell lines derived from human somatic cells Science 318 2007 1917 1920
72. W.E. Lowry, L. Richter, R. Yachechko, A.D. Pyle, J. Tchieu, R. Sridharan, A.T. Clark, and K. Plath Generation of human induced pluripotent stem cells from dermal fibroblasts Proc. Natl. Acad. Sci. U. S. A. 105 2008 2883 2888 (Pubitemid 351723638)
73. I.H. Park, R. Zhao, J.A. West, A. Yabuuchi, H. Huo, T.A. Ince, P.H. Lerou, M.W. Lensch, and G.Q. Daley Reprogramming of human somatic cells to pluripotency with defined factors Nature 451 2008 141 146
74. M. Dejosez, J.S. Krumenacker, L.J. Zitur, M. Passeri, L.F. Chu, Z. Songyang, J.A. Thomson, and T.P. Zwaka Ronin is essential for embryogenesis and the pluripotency of mouse embryonic stem cells Cell 133 2008 1162 1174 (Pubitemid 351852919)
75. S. Nagata, M. Toyoda, S. Yamaguchi, K. Hirano, H. Makino, K. Nishino, Y. Miyagawa, H. Okita, N. Kiyokawa, M. Nakagawa, S. Yamanaka, H. Akutsu, A. Umezawa, and T. Tada Efficient reprogramming of human and mouse primary extra-embryonic cells to pluripotent stem cells Genes Cells 14 2009 1395 1404
76. D. Huangfu, K. Osafune, R. Maehr, W. Guo, A. Eijkelenboom, S. Chen, W. Muhlestein, and D.A. Melton Induction of pluripotent stem cells from primary human fibroblast with only oct4 and sox2 Nat. Biotech. 26 2008 1269 1275
77. K. Schenke-Layland, K.E. Rhodes, E. Angelis, Y. Butylkova, S. Hyderkhan-Hagvall, C. Gekas, R. Zhang, J.I. Goldhabber, H.K. Mikkola, K. Plath, and W.R. MacLellan Reprogrammed mouse fibroblasts differentiate into cells of cardiovascular and hematopoietic lineages Stem Cells 26 2008 1537 1546
78. G. Narazaki, H. Uosaki, M. Teranishi, K. Okita, B. Kim, S. Matsuoka, S. Yamanaka, and J.K. Yamashita Directed and systemic differentiation of cardiovascular cells from mouse induced pluripotent cells Circulation 118 2008 498 506
79. J. Zhang, G.F. Wilson, A.G. Soerens, C.H. Koonce, J. Yu, S.P. Palecek, J.A. Thomson, and T.J. Kamp Functional cardiomyocytes derived from human induced pluripotent stem cells Circ. Res. 104 2009 e30 e41
80. M.H. Chin, M.J. Mason, W. Xie, S. Volinia, M. Singer, C. Peterson, G. Ambartsumyan, O. Aimiuwu, L. Richter, J. Zhang, I. Khvorostov, V. Ott, M. Grunstein, N. Lavon, N. Benvenisty, C.M. Croce, A.T. Clark, T. Baxter, A.D. Pyle, M.A. Teitell, M. Pelegrini, K. Plath, and W.E. Lowry Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures Cell Stem Cell 5 2009 111 123
81. A. Doi, I.H. Park, B. Wen, P. Murakami, M.J. Aryee, R. Irizarry, B. Herb, C. Ladd-Acosta, J. Rho, S. Loewer, J. Miller, T. Schlaeger, G.Q. Daley, and A.P. Feinberg Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts Nat. Genet. 41 2009 1350 1353
82. J. Deng, R. Shoemaker, B. Xie, A. Gore, E.M. LeProust, J. Antosiewicz-Bourget, D. Egli, N. Maherali, I.H. Park, J. Yu, G.Q. Daley, K. Eggan, K. Hochedlinger, J. Thomson, W. Wang, Y. Gao, and K. Zhang Targeted bisulfate sequencing reveals changes in DNA methylation associated with nuclear reprogramming Nat. Biotechnol. 27 2009 353 360
83. J.S. Krumenacker, S. Katsuki, A. Kots, and F. Murad Differential expression of genes involved in cGMP-dependent nitric oxide signaling in murine embryonic stem (ES) cells and cell-derived cardiomyocytes Nitric Oxide 14 2006 1 11 (Pubitemid 43063502)
84. K. Mujoo, J.S. Krumenacker, Y. Wada, and F. Murad Differential expression of nitric oxide signaling components in undifferentiated and differentiated human embryonic stem cells Stem Cells Dev. 15 2006 779 787 (Pubitemid 46147850)
85. K. Mujoo, V. Sharin, N. Bryan, J.S. Krumenacker, C. Sloan, S. Parveen, A. Kots, and F. Murad Role of nitric oxide signaling components in differentiation of embryonic stem cells to myocardial cells Proc. Natl. Acad. Sci. U. S. A. 105 2008 18924 18929
86. V. Sharin, K. Mujoo, A. Kots, E. Martin, F. Murad, and I. Sharina Nitric oxide receptor soluble guanylyl cyclase undergoes splicing regulation in differentiating human embryonic stem cells Stem Cells Dev. 20 2011 1287 1293
87. J.S. Krumenacker, and F. Murad NO-cGMP signaling in development and stem cells Mol. Genet. Metab. 87 2006 311 314
88. K.S. Madhusoodnan, and F. Murad NO-cGMP signaling and regenerative medicine involving stem cells Neurochem. Res. 32 2007 681 694 (Pubitemid 46481298)
89. Madhusoodanan, K.S.; Mujoo, K.; Murad, F. Expression and localization of guanylyl cyclases during the differentiation of embryonic stem cells into neural precursor cells using a novel and highly efficient method. In 8th ISSCR meeting, San Francisco, 16-19 June 2010, poster session abstracts, p. 215.
90. P.J. Shami, and J.B. Weinberg Differential effects of nitric oxide on erythroid and myeloid colony growth from CD34+ human bone marrow cells Blood 87 1996 977 982 (Pubitemid 26043528)
91. A. Bøyum, H.B. Fjerdingstad, V.A. Tennfjord, H.B. Benestad, and D. Løvhaug Specific antibodies to mouse Sca-1- (Ly-6A/E) or Thy-1-positive haematopoietic progenitor cells induce formation of nitric oxide which inhibits subsequent colony formation Eur. J. Haematol. 73 2004 427 430 (Pubitemid 39564366)
92. T. Michurina, P. Krasnov, A. Balazs, N. Nakaya, T. Vasilieva, B. Kuzin, N. Khrushchov, R.C. Mulligan, and G. Enikolopov Nitric oxide is a regulator of hematopoietic stem cell activity Mol. Ther. 10 2004 241 248 (Pubitemid 39117870)
93. A. Aicher, C. Heeschen, C. Mildner-Rihm, C. Urbich, C. Ihling, K. Technau-Ihling, A.M. Zeiher, and S. Dimmeler Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells Nat. Med. 11 2003 1370 1376 (Pubitemid 37466185)
94. S.M. Guthrie, L.M. Curtis, R.N. Mames, G.G. Simon, M.B. Grant, and E.W. Scott The nitric oxide pathway modulates hemangioblast activity of adult hematopoietic stem cells Blood 105 2005 1916 1922 (Pubitemid 40731772)
95. W. Bloch, B.K. Fleischmann, D.E. Lorke, C. Andressen, B. Hops, J. Hescheler, and K. Addicks Nitric oxide synthase expression and role during cardiomyogenesis Cardiovasc. Res. 43 1999 675 684 (Pubitemid 29369266)
96. S. Kanno, P.K.M. Kim, K. Sallam, J. Lei, T.R. Billiar, and L.L. Shears II Nitric oxide facilitates cardiomyogenesis in mouse embryonic stem cells Proc. Natl. Acad. Sci. U. S. A. 101 2004 12277 12281 (Pubitemid 39145434)
97. S. Kloss, H. Furneaux, and A. Mülsch Post-transcriptional regulation of soluble guanylyl cyclase expression in rat aorta J. Biol. Chem. 278 2003 2377 2383 (Pubitemid 36801310)
98. M.L. Marro, C. Peiró, C.M. Panayiotou, R.S. Baliga, S. Meurer, H.H. Schmidt, and A.J. Hobbs Characterization of the human alpha1 beta1 soluble guanylyl cyclase promoter: key role for NF-kappaB(p50) and CCAAT-binding factors in regulating expression of the nitric oxide receptor J. Biol. Chem. 283 2008 20027 20036
99. I.G. Sharina, E. Martin, A. Thomas, K.L. Uray, and F. Murad CCAAT-binding factor regulates expression of the beta 1 subunit of soluble guanylyl cyclase gene in the BE-2 human neuroblastoma cell line Proc. Natl. Acad. Sci. U. S. A. 100 2003 11523 11528 (Pubitemid 37205969)
100. Z. Zhou, N. Sayed, A. Pyriochou, C. Roussos, D. Fulton, A. Beuve, and A. Papapetropoulos Protein kinase G phosphorylates soluble guanylyl cyclase on serine 64 and inhibits its activity Arterioscler. Thromb. Vasc. Biol. 10 2008 1803 1810
101. J.P. Cabilla, S.A. Ronchetti, S.I. Nudler, E.A. Miler, F.A. Quinteros, and B.H. Duvilanski Nitric oxide-sensitive guanylyl cyclase subunit expression changes during estrous cycle in anterior pituitary glands Am. J. Physiol. Endocrinol. Metab. 296 2009 E731 E737
102. D.Y. Zhu, and Y.J. Lou Icariin-mediated expression of cardiac genes and modulation of nitric oxide signaling pathway during differentiation of mouse embryonic stem cells into cardiomyocytes in vitro Acta Pharmacol. Sin. 27 2006 311 320
103. W. Pan, L.D. Quarles, L.H. Song, Y.H. Yu, C. Jiao, H.B. Tang, C.H. Jiang, H.W. Deng, Y.J. Li, H.H. Zhou, and Z.S. Xiao Genistein stimulates the osteoblastic differentiation via NO/cGMP in bone marrow culture J. Cell. Biochem. 94 2005 307 316 (Pubitemid 41420309)
104. Mujoo, K.; Nikonoff, L.E.; Kots, A.Y.; Murad, F. Curcumin: a plant derived compound induces differentiation of human embryonic stem cells into myocardial cells; possible role of nitric oxide pathway. Abstract presented at 8th ISSCR meeting held at San Francisco, CA, June 16-19, 2010, page 38-poster session abstracts
105. K. Mora-Castilla, J.R. Tejedo, A. Hmadcha, G.M. Cahuana, F. Martin, B. Soria, and F.J. Bedoya Nitric oxide repression of Nanog promotes mouse embryonic stem cell differentiation Cell Death Differ. 17 2010 1025 1033
106. J.R. Tejedo, R. Tapia-Limonchi, S. Mora-Castilla, G.M. Cahuana, A. Hmadcha, F. Martin, F.J. Bedoya, and B. Soria Low concentrations of nitric oxide delay the differentiation of embryonic stem cells and promote their survival Cell Death Dis. 1 2010 e80
107. U. Gomez-Pinedo, R. Rodrigo, O. Cauli, S. Herraiz, J.M. Garcia-Verdugo, B. Pellicer, A. Pellicer, and V. Filipo cGMP modulates stem cell differentiation to neurons in brain in vivo Neuroscience 165 2010 1275 1283
108. J.C. Wong, and R.R. Ficus Essential role of nitric oxide(NO)/cGMP/protein kinase G type-1 α (PKG-1 α) signaling pathway and arterial natriuretic peptide (ANP)/cGMP/PKG-1 α autocrine loop in promoting proliferation and cell survival of OP9 bone marrow stromal cells J. Cell. Biochem. 112 2011 829 839
109. S. Mobley, J.S. Shookhof, K. Foshay, M. Park, and G.I. Gallicano PKG and PKC are downregulated during cardiomyocyte differentiation from embryonic stem cells: manipulation of these pathways enhances cardiomyocyte production Stem Cells Int. 2010 2010 701212
110. C. Foresta, A. Cabrelle, M. Ferigo, N. Caretta, A. Garolla, G. Palu, and A. Ferlin PDE-5 inhibitor Vardenafil, increases circulating progenitor cells in humans Int. J. Impot. Res. 17 2005 377 380 (Pubitemid 41025774)
111. M. Pekkinen, M.E. Ahlstrom, U. Riehel, M.M. Huttunen, and C.J. Lamberg-Allardt Effect of phosphodiesterase 7 inhibition by RNA interference on the gene expression and differentiation of human mesenchymal stem cell-derived osteoblasts Bone 43 2008 84 90
112. M. Zhang, E. Takimoto, S. Hsu, D.I. Lee, T. Nagayama, T. Danner, N. Koitabashi, A.S. Barth, D. Bedja, K.L. Gabrielson, Y. Wang, and D.A. Kass Myocardial remodeling is controlled by myocyte-targeted gene regulation of phosphodiesterase type 5 J. Am. Coll. Cardiol. 56 2010 2021 2030
113. F. Spallotta, J. Rosati, S. Straino, S. Nanni, A. Grasselli, V. Ambrosino, D. Rotili, S. Valente, A. Farsetti, A. Mai, M.C. Capogrossi, C. Gaetano, and B. Illi Nitric oxide determines mesodermic differentiation of mouse embryonic stem cells by activating class IIa histone deacetylases: potential therapeutic implications in a mouse model of hindlimb ischemia Stem Cells 28 2010 431 442
114. Y. Liu, J. Song, W. Liu, Y. Wan, X. Chen, and C. Hu Growth and differentiation of rat bone marrow stromal cells: does 5-azacytidine trigger their cardiomyogenic differentiation? Cardiovasc. Res. 58 2003 460 468 (Pubitemid 36570404)
115. H. Reinecke, V. Poppa, and C.E. Murry Skeletal muscle stem cells do not transdifferentiate into cardiomyocytes after cardiac grafting J. Mol. Cell. Cardiol. 34 2002 241 249 (Pubitemid 35222833)
116. A.J. Wagers, R.I. Sherwood, J.L. Christensen, and I.L. Weissman Little evidence for developmental plasticity of adult hematopoietic stem cells Science 297 2002 2256 2259
117. J.Y. Min, Y. Yang, K.L. Converso, L. Liu, Q. Huang, J.P. Morgan, and Y.F. Xaio Transplantation of embryonic stem cells improves cardiac function in postinfarcted rats J. Appl. Physiol. 92 2002 288 296 (Pubitemid 34670018)
118. J.Y. Min, Y. Yang, M.F. Sullivan, Q. Ke, K.L. Converso, Y. Chen, J.P. Morgan, and Y.F. Xiao Long-term improvement of cardiac function in rats after infarction by transplantation of embryonic stem cells J. Thorac. Cardiovasc. Surg. 125 2003 361 369 (Pubitemid 36228314)
119. H. Naito, S. Taniguchi, and T. Kawata Embryonic stem cell-derived cardiomyocyte transplantation into the infarcted myocardium Heart Surg. Forum 6 2002 1
120. A. Behfar, L.V. Zingman, D.M. Hodgson, J.M. Rauzier, G.C. Kane, A. Terzic, and M. Puceat Stem cell differentiation requires a paracrine pathway in the heart FASEB J. 16 2002 1558 1566 (Pubitemid 35154638)
121. Y. Yang, J.Y. Min, J.S. Rana, Q. Ke, J. Cai, Y. Chen, J.P. Morgan, and Y.F. Xiao VEGF enhances functional improvement of postinfarcted hearts by transplantation of ESC-differentiated cells J. Appl. Physiol. 93 2002 1140
122. C. Kupatt, R. Hinkel, R. Vachenauer, J. Horstkotte, P. Raake, T. Sandner, R. Kreuzpointner, F. Muller, S. Dimmeler, O. Feron, and P. Boekstegers VEGF165 transfection decreases postischemic NF-κB-dependent myocardial reperfusion injury in vivo: role of eNOS phosphorylation FASEB J. 17 2003 705 707
123. R. Gyurko, P. Kuhlencordt, M.C. Fishman, and P.L. Huang Modulation of mouse cardiac function in vivo by eNOS and ANP Am. J. Physiol. Heart Circ. Physiol. 278 2000 H971 H981
124. S. Hoshida, N. Yamashita, J. Igarashi, M. Nishida, M. Hori, T. Kamada, T. Kuzuya, and M. Tada Nitric oxide synthase protects the heart against ischemia-reperfusion injury in rabbits J. Pharmacol. Exp. Ther. 274 1995 413 418
125. X. Zhao, X. Lu, and Q. Feng Deficiency in endothelial nitric oxide synthase impairs myocardial angiogenesis Am. J. Physiol. Heart Circ. Physiol. 283 2002 H2371 H2378
126. D. Wang, X.P. Yang, Y.H. Liu, O.A. Carretero, and M.C. LaPointe Reduction of myocardial infarct size by inhibition of inducible nitric oxide synthase Am. J. Hypertens. 12 1999 174 182 (Pubitemid 29130419)
127. S.M. Wildhirt, R.R. Dudek, H. Suzuki, and R.J. Bing Involvement of inducible nitric oxide synthase in the inflammatory process of myocardial infarction Int. J. Cardiol. 50 1995 253 261
128. S. Janssens, P. Pokreisz, L. Schoonjans, M. Pellens, P. Vermeersch, M. Tjwa, P. Jans, M. Scherrer-Crosbie, M.H. Picard, Z. Szelid, H. Gillijns, F. Van de Werf, D. Collen, and K.D. Bloch Cardiomyocyte-specific overexpression of nitric oxide synthase 3 improves left ventricular performance and reduces compensatory hypertrophy after myocardial infarction Circ. Res. 94 2004 1256 1262 (Pubitemid 38656413)
129. T. Damy, P. Ratajczak, E. Robidel, J.K. Bendall, P. Oliviero, J. Boczkowski, T. Ebrahimian, F. Marotte, J.-L. Samuel, and C. Heymes Up-regulation of cardiac nitric oxide synthase 1-derived nitric oxide after myocardial infarction in senescent rats FASEB J. 17 2003 1934 1936
130. A. Calderone, C.M. Thaik, M. Takahashi, D.L. Chang, and W.S. Colucci Nitric oxide, atrial natriuretic peptide, and cGMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts J. Clin. Invest. 101 1998 812 818 (Pubitemid 28096078)
131. Y. Ishigai, T. Mori, T. Ikeda, A. Fukuzawa, and T. Shibano Role of bradykinin-NO pathway in prevention of cardiac hypertrophy by ACE inhibitor in rat cardiomyocytes Am. J. Physiol. 273 1997 H2659 H2663
132. K.C. Wollert, B. Fiedler, S. Gambaryan, A. Smolenski, J. Heineke, E. Butt, C. Trautwein, S.M. Lohmann, and H. Drexler Gene transfer of cGMP-dependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes Hypertension 39 2002 87 92 (Pubitemid 34098094)
133. J. Dulak, A. Jozkowicz, I. Guevara, and A. Dembinska-Kiec Gene transfer of vascular endothelial growth factor and endothelial nitric oxide synthase-implications for gene therapy in cardiovascular diseases Pol. J. Pharmacol. 51 1999 233 241 (Pubitemid 29245575)
134. I. Kishimoto, K. Rossi, and D.L. Garbers A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy Proc. Natl. Acad. Sci. U. S. A. 98 2001 2703 2706 (Pubitemid 32209546)
135. A. Zahabi, S. Picard, N. Fortin, T.L. Reudelhuber, and C.F. Deschepper Expression of constitutively active guanylate cyclase in cardiomyocytes inhibits the hypertrophic effects of isoproterenol and aortic constriction on mouse hearts J. Biol. Chem. 278 2003 47694 47699 (Pubitemid 37523215)
136. B. Fiedler, S.M. Lohmann, A. Smolenski, S. Linnemuller, B. Pieske, F. Schroder, J.D. Molkentin, H. Drexler, and K.C. Wollert Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes Proc. Natl. Acad. Sci. U. S. A. 99 2002 11363 11368 (Pubitemid 34920931)
137. J.W. Knowles, G. Esposito, L. Mao, J.R. Hagaman, J.E. Fox, O. Smithies, H.A. Rockman, and N. Maeda Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice J. Clin. Invest. 107 2001 975 984 (Pubitemid 32328002)
138. E. Leontiadis, A. Manginas, and D.V. Cokkinos Cardiac repair-fact or fancy? Heart Fail. Rev. 11 2006 155 170
139. T. Kofidis, J.L. de Bruin, T. Yamane, M. Tanaka, D.R. Lebl, R.J. Swijnenburg, I.L. Weissman, and R.C. Robbins Stimulation of paracrine pathways with growth factors enhances embryonic stem cell engraftment and host-specific differentiation in the heart after ischemic myocardial injury Circulation 111 2005 2486 2493 (Pubitemid 40696137)
140. D. Kumar, T.J. Kamp, and M.M. Lewinter Embryonic stem cells: differentiation into cardiomyocytes and potential for heart repair and regeneration Coron. Artery Dis. 16 2005 111 116 (Pubitemid 40393186)
141. K.L. Laugwitz, A. Moretti, J. Lam, P. Gruber, Y. Chen, S. Woodard, L.Z. Lin, C.L. Cai, M.M. Lu, M. Reth, O. Platoshyn, J.X. Yuan, S. Evans, and K.R. Chien Post natal Isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages Nature 433 2005 647 653 (Pubitemid 40282999)
142. A.M. Smits, P. Vliet, R.J. Hassink, M.-J. Goumans, and P.A. Doevendans The role of stem cells in cardiac regeneration J. Cell. Mol. Med. 9 2005 25 36
143. N. Li, X. Lu, X. Zhao, F.L. Xiang, A. Xenocostas, M. Karmazyn, and Q. Feng Endothelial nitric oxide synthase promotes bone marrow stromal cell migration to the ischemic myocardium via upregulation of stromal cell-derived factor-1alpha Stem Cells 27 2009 961 970
144. Y.C. Lin, S. Leu, C.K. Sun, C.H. Yen, Y.H. Kao, L.T. Chang, T.H. Tsai, S. Chua, M. Fu, S.F. Ko, C.J. Wu, F.Y. Lee, and H.K. Yip Early combined treatment with sildenafil and adipose-derived mesenchymal stem cells preserves heart function in rat dilated cardiomyopathy J. Transl. Med. 8 2010 88
145. L.W. van Laake, R. Passier, J. Monshouwer-Kloots, A.J. Verkleij, D.J. Lips, C. Freund, K. den Ouden, D. Ward-van Oostwaard, J. Korving, L.G. Tertoolen, C.J. van Echteld, P.A. Doevendans, and C.L. Mummery Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction Stem Cell Res. 1 2007 9 24 (Pubitemid 350251944)
146. L.W. van Laake, R. Passier, K. Den Ouden, C. Schreurs, J. Monshouwer-Kloots, D. Ward-van Oostwaard, C.J. van Echteld, P.A. Doevendans, and C.L. Mummery Improvement of mouse cardiac function by hESC-derived cardiomyocytes correlates with vascularity but not graft size Stem Cell Res. 3 2009 106 112
147. S.R. Braam, R. Passier, and C.L. Mummery Cardiomyocytes from human pluripotent stem cells in regenerative medicine and drug discovery Trends Pharmacol. Sci. 30 2009 536 545