Skip to main content

Advertisement

SpringerLink
Log in

Nitric oxide regulates multiple functions and fate of adult progenitor and stem cells

  • Mini Review
  • Published:
Journal of Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Nitric oxide is an endogenous gas which exerts autocrine/paracrine actions by different signaling pathways and/or direct interactions with intracellular compounds and structures. Several processes are regulated by nitric oxide in stem cells including self-renewal, viability, migration, proliferation, and differentiation. The modulation of cell functions depends on its concentrations because opposite effects can be observed when low and high levels of nitric oxide are compared. Here, the responses to nitric oxide of adult stem/progenitor cells which are often used in regenerative medicine, including mesenchymal stem cells, hematopoietic stem cells, neural stem cells, endothelial progenitor cells, satellite cells, and fibro-adipogenic precursor cells, are reviewed. Therapeutic strategies which employ drugs releasing nitric oxide or modulating nitric oxide intracellular pathways are suggested to perform new ex vivo preconditioning or in vivo treatments suitable for stem/progenitor cell therapy and tissue engineering applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9:1370–1376

    CAS  PubMed  Google Scholar 

  2. Alagesan S, Griffin MD (2014) Autologous and allogeneic mesenchymal stem cells in organ transplantation: what do we know about their safety and efficacy? Curr Opin Organ Transp 19:65–72

    CAS  Google Scholar 

  3. Aleksinskaya MA, van Faassen EE, Nelissen J, Janssen BJ, De Mey J, Hanemaaijer R, Rabelink T, van Zonneveld AJ (2013) Identification of free nitric oxide radicals in rat bone marrow: implications for progenitor cell mobilization in hypertension. PLoS One 8:e57761

    PubMed Central  CAS  PubMed  Google Scholar 

  4. Ali G, Mohsin S, Khan M, Nasir GA, Shams S, Khan SN, Riazuddin S (2012) Nitric oxide augments mesenchymal stem cell ability to repair liver fibrosis. J Transl Med 10:75

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Ascenzi P, di Masi A, Sciorati C, Clementi E (2010) Peroxynitrite—an ugly biofactor? Biofactors 36:264–273

    CAS  PubMed  Google Scholar 

  6. Barra N, del Castillo JR, Troncy E (2011) Involvement of the nitric oxide-soluble guanylyl cyclase pathway in the oxytocin-mediated differentiation of porcine bone marrow stem cells into cardiomyocytes. Nitric Oxide 24:25–33

    Google Scholar 

  7. Bassaneze V, Barauna VG, Lavini-Ramos C, Kalil J, Schettert IT, Miyakawa AA, Krieger JE (2010) Shear stress induces nitric oxide-mediated vascular endothelial growth factor production in human adipose tissue mesenchymal stem cells. Stem Cells Dev 19:371–378

    CAS  PubMed  Google Scholar 

  8. Bergsland M, Covacu R, Perez Estrada C, Svensson M, Brundin L (2014) Nitric oxide-induced neuronal to glial lineage fate-change depends on NRSF/REST function in neural progenitor cells. Stem Cells 32:2539–2549

    CAS  PubMed  Google Scholar 

  9. Bian K, Doursout MF, Murad F (2008) Vascular system: role of nitric oxide in cardiovascular diseases. J Clin Hypertens (Greenwich) 10:304–310

    CAS  Google Scholar 

  10. Blau HM, Webster C, Pavlath GK (1983) Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 80:4856–4860

    PubMed Central  CAS  PubMed  Google Scholar 

  11. Buono R, Vantaggiato C, Pisa V, Azzoni E, Bassi MT, Brunelli S, Sciorati C, Clementi E (2012) Nitric oxide sustains long-term skeletal muscle regeneration by regulating fate of satellite cells via signaling pathways requiring Vangl2 and cyclic GMP. Stem Cells 30:197–209

    PubMed Central  CAS  PubMed  Google Scholar 

  12. Burke AJ, Sullivan FJ, Giles FJ, Glynn SA (2013) The yin and yang of nitric oxide in cancer progression. Carcinogenesis 34:503–512

    CAS  PubMed  Google Scholar 

  13. Capanni C, Squarzoni S, Petrini S, Villanova M, Muscari C, Maraldi NM, Guarnieri C, Caldarera CM (1998) Increase of neuronal nitric oxide synthase in rat skeletal muscle during ageing. Biochem Biophys Res Commun 245:216–219

    CAS  PubMed  Google Scholar 

  14. Carreira BP, Morte MI, Lourenço AS, Santos AI, Inácio A, Ambrósio AF, Carvalho CM, Araújo IM (2013) Differential contribution of the guanylyl cyclase-cyclic GMP-protein kinase G pathway to the proliferation of neural stem cells stimulated by nitric oxide. Neurosignals 21:1–13

    CAS  PubMed  Google Scholar 

  15. Cepinskas G, Rui T, Kvietys PR (2002) Interaction between reactive oxygen metabolites and nitric oxide in oxidant tolerance. Free Radic Biol Med 33:433–440

    CAS  PubMed  Google Scholar 

  16. Chen X, Gan Y, Li W, Su J, Zhang Y, Huang Y, Roberts AI, Han Y, Li J, Wang Y, Shi Y (2014) The interaction between mesenchymal stem cells and steroids during inflammation. Cell Death Dis 5:e1009

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Choudhari SK, Chaudhary M, Bagde S, Gadbail AR, Joshi V (2013) Nitric oxide and cancer: a review. World J Surg Oncol 11:118

    PubMed  Google Scholar 

  18. Chu L, Jiang Y, Hao H, Xia Y, Xu J, Liu Z, Verfaillie CM, Zweier JL, Liu Z (2008) Nitric oxide enhances Oct-4 expression in bone marrow stem cells and promotes endothelial differentiation. Eur J Pharmacol 591:59–65

    CAS  PubMed  Google Scholar 

  19. Cordani N, Pisa V, Pozzi L, Sciorati C, Clementi E (2014) Nitric oxide controls fat deposition in dystrophic skeletal muscle by regulating fibro-adipogenic precursor differentiation. Stem Cells 32:874–885

    CAS  PubMed  Google Scholar 

  20. Curtis BM, Leix KA, Ji Y, Glaves RS, Ash DE, Mohanty DK (2014) Slow and sustained nitric oxide releasing compounds inhibit multipotent vascular stem cell proliferation and differentiation without causing cell death. Biochem Biophys Res Commun 450:208–212

    CAS  PubMed  Google Scholar 

  21. de Nigris F, Balestrieri ML, Williams-Ignarro S, D’Armiento FP, Lerman LO, Byrns R, Crimi E, Palagiano A, Fatigati G, Ignarro LJ, Napoli C (2007) Therapeutic effects of autologous bone marrow cells and metabolic intervention in the ischemic hindlimb of spontaneously hypertensive rats involve reduced cell senescence and CXCR4/Akt/eNOS pathways. J Cardiovasc Pharmacol 50:424–433

    PubMed  Google Scholar 

  22. De Palma C, Clementi E (2012) Nitric oxide in myogenesis and therapeutic muscle repair. Mol Neurobiol 46:682–692

    CAS  PubMed  Google Scholar 

  23. De Palma C, Falcone S, Pisoni S, Cipolat S, Panzeri C, Pambianco S, Pisconti A, Allevi R, Bassi MT, Cossu G, Pozzan T, Moncada S, Scorrano L, Brunelli S, Clementi E (2010) Nitric oxide inhibition of Drp1-mediated mitochondrial fission is critical for myogenic differentiation. Cell Death Differ 17:1684–1696

    PubMed Central  PubMed  Google Scholar 

  24. Defawe OD, Kim S, Chen L, Huang D, Kenagy RD, Renné T, Walter U, Daum G, Clowes AW (2010) VASP phosphorylation at serine239 regulates the effects of NO on smooth muscle cell invasion and contraction of collagen. J Cell Physiol 222:230–237

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Derbyshire ER, Marletta MA (2012) Structure and regulation of soluble guanylate cyclase. Annu Rev Biochem 81:533–559

    CAS  PubMed  Google Scholar 

  26. Erusalimsky JD, Moncada S (2007) Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 27:2524–2531

    CAS  PubMed  Google Scholar 

  27. Fernández Vallone VB, Romaniuk MA, Choi H, Labovsky V, Otaegui J, Chasseing NA (2013) Mesenchymal stem cells and their use in therapy: what has been achieved? Differentiation 85:1–10

    PubMed  Google Scholar 

  28. Finanger Hedderick EL, Simmers JL, Soleimani A, Andres-Mateos E, Marx R, Files DC, King L, Crawford TO, Corse AM, Cohn RD (2011) Loss of sarcolemmal nNOS is common in acquired and inherited neuromuscular disorders. Neurology 76:960–967

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Fiumana E, Pasquinelli G, Foroni L, Carboni M, Bonafé F, Orrico C, Nardo B, Tsivian M, Neri F, Arpesella G, Guarnieri C, Caldarera CM, Muscari C (2013) Localization of mesenchymal stem cells grafted with a hyaluronan-based scaffold in the infarcted heart. J Surg Res 179:e21–e29

    CAS  PubMed  Google Scholar 

  30. Fuseler JW, Valarmathi MT (2012) Modulation of the migration and differentiation potential of adult bone marrow stromal stem cells by nitric oxide. Biomaterials 33:1032–1043

    CAS  PubMed  Google Scholar 

  31. Fussen S, De Boeck BW, Zellweger MJ, Bremerich J, Goetschalckx K, Zuber M, Buser PT (2011) Cardiovascular magnetic resonance imaging for diagnosis and clinical management of suspected cardiac masses and tumours. Eur Heart J 32:1551–1560

    PubMed  Google Scholar 

  32. Ghasemi A, Mehrazin F, Zahediasl S (2013) Effect of nitrate and l-arginine therapy on nitric oxide levels in serum, heart, and aorta of fetal hypothyroid rats. J Physiol Biochem 69:751–759

    CAS  PubMed  Google Scholar 

  33. Ghasemi M, Fatemi A (2014) Pathologic role of glial nitric oxide in adult and pediatric neuroinflammatory diseases. Neurosci Biobehav Rev 45C:168–182

    Google Scholar 

  34. Ghosh S, George S, Roy U, Ramachandran D, Kolthur-Seetharam U (2010) NAD: a master regulator of transcription. Biochim Biophys Acta 1799:681–693

    CAS  PubMed  Google Scholar 

  35. Giordano E, Flamigni F, Guarnieri C, Muscari C, Pignatti C, Stefanelli C, Tantini B, Caldarera CM (2010) Polyamines in cardiac physiology and disease. Open Heart Fail J 3:25–30

    CAS  Google Scholar 

  36. Govoni M, Muscari C, Guarnieri C, Giordano E (2013) Mechanostimulation protocols for cardiac tissue engineering. Biomed Res Int 2013:918640

    PubMed Central  PubMed  Google Scholar 

  37. Hammond J, Balligand JL (2012) Nitric oxide synthase and cyclic GMP signaling in cardiac myocytes: from contractility to remodeling. J Mol Cell Cardiol 52:330–340

    CAS  PubMed  Google Scholar 

  38. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625–637

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Hirst DG, Robson T (2011) Nitric oxide physiology and pathology. Methods Mol Biol 704:1–13

    CAS  PubMed  Google Scholar 

  40. Hoang HH, Padgham SV, Meininger CJ (2013) L-arginine, tetrahydrobiopterin, nitric oxide and diabetes. Curr Opin Clin Nutr Metab Care 16:76–82

    CAS  PubMed  Google Scholar 

  41. Hofner M, Höllrigl A, Puz S, Stary M, Weitzer G (2007) Desmin stimulates differentiation of cardiomyocytes and upregulation of brachyury and nkx2.5. Differentiation 75:605–615

    CAS  PubMed  Google Scholar 

  42. Hu J, Mahmoud MI, el-Fakahany EE (1994) Polyamines inhibit nitric oxide synthase in rat cerebellum. Neurosci Lett 175:41–45

    CAS  PubMed  Google Scholar 

  43. Huang L, Qiu N, Zhang C, Wei HY, Li YL, Zhou HH, Xiao ZS (2008) Nitroglycerin enhances proliferation and osteoblastic differentiation in human mesenchymal stem cells via nitric oxide pathway. Acta Pharmacol Sin 29:580–586

    PubMed  Google Scholar 

  44. Imanishi Y, Saito A, Komoda H, Kitagawa-Sakakida S, Miyagawa S, Kondoh H, Ichikawa H, Sawa Y (2008) Allogenic mesenchymal stem cell transplantation has a therapeutic effect in acute myocardial infarction in rats. J Mol Cell Cardiol 44:662–671

    PubMed  Google Scholar 

  45. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM (2002) Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896–904

    CAS  PubMed  Google Scholar 

  46. Joiner DM, Tayim RJ, Kadado A, Goldstein SA (2012) Bone marrow stromal cells from aged male rats have delayed mineralization and reduced response to mechanical stimulation through nitric oxide and ERK1/2 signaling during osteogenic differentiation. Biogerontology 13:467–478

    CAS  PubMed  Google Scholar 

  47. Joubert J, Malan SF (2011) Novel nitric oxide synthase inhibitors: a patent review. Expert Opin Ther Pat 21:537–560

    CAS  PubMed  Google Scholar 

  48. Kanki-Horimoto S, Horimoto H, Mieno S, Kishida K, Watanabe F, Furuya E, Katsumata T (2006) Synthetic vascular prosthesis impregnated with mesenchymal stem cells overexpressing endothelial nitric oxide synthase. Circulation 114(1 Suppl):I327–I330

    PubMed  Google Scholar 

  49. Kanki-Horimoto S, Horimoto H, Mieno S, Kishida K, Watanabe F, Furuya E, Katsumata T (2006) Implantation of mesenchymal stem cells overexpressing endothelial nitric oxide synthase improves right ventricular impairments caused by pulmonary hypertension. Circulation 114(1 Suppl):I181–I185

    PubMed  Google Scholar 

  50. Karam JP, Muscari C, Montero-Menei CN (2012) Combining adult stem cells and polymeric devices for tissue engineering in infarcted myocardium. Biomaterials 33:5683–5695

    CAS  PubMed  Google Scholar 

  51. Karam JP, Muscari C, Sindji L, Bastiat G, Bonafè F, Venier-Julienne MC, Montero-Menei NC (2014) Pharmacologically active microcarriers associated with thermosensitive hydrogel as a growth factor releasing biomimetic 3D scaffold for cardiac tissue-engineering. J Control Release 192:82–94

    CAS  PubMed  Google Scholar 

  52. Kirton JP, Xu Q (2010) Endothelial precursors in vascular repair. Microvasc Res 79:193–199

    CAS  PubMed  Google Scholar 

  53. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19:541–564

    CAS  PubMed  Google Scholar 

  54. Lehmann J (2000) Nitric oxide donors—current trends in therapeutic applications. Expert Opin Ther Pat 10:559–574

    CAS  Google Scholar 

  55. Lei J, Vodovotz Y, Tzeng E, Billiar TR (2013) Nitric oxide, a protective molecule in the cardiovascular system. Nitric Oxide 35:175–185

    CAS  PubMed  Google Scholar 

  56. Li D, Fang Y, Wang P, Shan W, Zuo Z, Xie L (2012) Autologous transplantation of adipose-derived mesenchymal stem cells attenuates cerebral ischemia and reperfusion injury through suppressing apoptosis and inducible nitric oxide synthase. Int J Mol Med 29:848–854

    CAS  PubMed  Google Scholar 

  57. Li HM, Liu L, Mei X, Chen H, Liu Z, Zhao X (2014) Overexpression of inducible nitric oxide synthase impairs the survival of bone marrow stem cells transplanted into rat infarcted myocardium. Life Sci 106:50–57

    CAS  PubMed  Google Scholar 

  58. Li N, Lu X, Zhao X, Xiang FL, Xenocostas A, Karmazyn M, Feng Q (2009) Endothelial nitric oxide synthase promotes bone marrow stromal cell migration to the ischemic myocardium via upregulation of stromal cell-derived factor-1alpha. Stem Cells 27:961–970

    CAS  PubMed  Google Scholar 

  59. Liu Z, Jiang Y, Hao H, Gupta K, Xu J, Chu L, McFalls E, Zweier J, Verfaillie C, Bache RJ (2007) Endothelial nitric oxide synthase is dynamically expressed during bone marrow stem cell differentiation into endothelial cells. Am J Physiol Heart Circ Physiol 293:H1760–H1765

    CAS  PubMed  Google Scholar 

  60. Lundberg JO, Weitzberg E, Gladwin MT (2008) The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7:156–167

    CAS  PubMed  Google Scholar 

  61. Luo CX, Zhu DY (2011) Research progress on neurobiology of neuronal nitric oxide synthase. Neurosci Bull 27:23–35

    CAS  PubMed  Google Scholar 

  62. Martínez-Ruiz A, Cadenas S, Lamas S (2011) Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med 51:17–29

    PubMed  Google Scholar 

  63. Mujoo K, Krumenacker JS, Murad F (2011) Nitric oxide-cyclic GMP signaling in stem cell differentiation. Free Radic Biol Med 51:2150–2157

    PubMed Central  CAS  PubMed  Google Scholar 

  64. Muscari C, Bonafé F, Carboni M, Govoni M, Stanic I, Gamberini C, Ricci F, Tazzari PL, Caldarera CM, Guarnieri C (2008) Difluoromethylornithine stimulates early cardiac commitment of mesenchymal stem cells in a model of mixed culture with cardiomyocytes. J Cell Biochem 103:1046–1052

    CAS  PubMed  Google Scholar 

  65. Muscari C, Bonafè F, Fiumana E, Oranges CM, Pinto V, Caldarera CM, Guarnieri C, Morselli PG (2013) Comparison between stem cells harvested from wet and dry lipoaspirates. Connect Tissue Res 54:34–40

    CAS  PubMed  Google Scholar 

  66. Muscari C, Bonafe’ F, Gamberini C, Giordano E, Tantini B, Fattori M, Guarnieri C, Caldarera CM (2004) Early preconditioning prevents the loss of endothelial nitric oxide synthase and enhances its activity in the ischemic/reperfused rat heart. Life Sci 74:1127–1137

    CAS  PubMed  Google Scholar 

  67. Muscari C, Bonafè F, Martin-Suarez S, Valgimigli S, Valente S, Fiumana E, Fiorelli F, Rubini G, Guarnieri C, Caldarera CM, Capitani O, Arpesella G, Pasquinelli G (2013) Restored perfusion and reduced inflammation in the infarcted heart after grafting stem cells with a hyaluronan-based scaffold. J Cell Mol Med 17:518–530

    PubMed Central  CAS  PubMed  Google Scholar 

  68. Muscari C, Capanni C, Giordano E, Stefanelli C, Bonavita F, Stanic I, Bonafè F, Caldarera CM, Guarnieri C (2010) Leupeptin preserves cardiac nitric oxide synthase 3 during reperfusion following long-term cardioplegia. J Surg Res 164:e27–e35

    CAS  PubMed  Google Scholar 

  69. Muscari C, Gamberini C, Basile I, Bonafé F, Valgimigli S, Capitani O, Guarnieri C, Caldarera CM (2010) Comparison between culture conditions improving growth and differentiation of blood and bone marrow cells committed to the endothelial cell lineage. Biol Proced Online 12:89–106

    PubMed Central  Google Scholar 

  70. Muscari C, Gamberini C, Carboni M, Basile I, Farruggia G, Bonafè F, Giordano E, Caldarera CM, Guarnieri C (2007) Different expression of NOS isoforms in early endothelial progenitor cells derived from peripheral and cord blood. J Cell Biochem 102:992–1001

    CAS  PubMed  Google Scholar 

  71. Muscari C, Giordano E, Bonafè F, Govoni M, Guarnieri C (2014) Strategies affording prevascularized cell-based constructs for myocardial tissue engineering. Stem Cells Int 2014:434169

    PubMed Central  PubMed  Google Scholar 

  72. Muscari C, Giordano E, Bonafè F, Govoni M, Pasini A, Guarnieri C (2013) Priming adult stem cells by hypoxic pretreatments for applications in regenerative medicine. J Biomed Sci 20:63

    PubMed Central  CAS  PubMed  Google Scholar 

  73. Muscari C, Grossi L, Giordano E, Ferrari D, Bonafe F, Guarnieri C, Caldarera CM (2003) Evaluation of nitric oxide release in the coronary effluent by a novel EPR technique: a study on isolated rat hearts subjected to cold cardioplegia and reperfusion. Life Sci 74:109–123

    CAS  PubMed  Google Scholar 

  74. Musilli C, Karam JP, Paccosi S, Muscari C, Mugelli A, Montero-Menei CN, Parenti A (2012) Pharmacologically active microcarriers for endothelial progenitor cell support and survival. Eur J Pharm Biopharm 81:609–616

    CAS  PubMed  Google Scholar 

  75. Mustafa AK, Gadalla MM, Snyder SH (2009) Signaling by gasotransmitters. Sci Signal 2:re2. doi: 10.1126/scisignal.268re2

  76. Napoli C, Paolisso G, Casamassimi A, Al-Omran M, Barbieri M, Sommese L, Infante T, Ignarro LJ (2013) Effects of nitric oxide on cell proliferation: novel insights. J Am Coll Cardiol 62:89–95

    CAS  PubMed  Google Scholar 

  77. Naseem KM, Riba R (2008) Unresolved roles of platelet nitric oxide synthase. J Thromb Haemost 6:10–19

    CAS  PubMed  Google Scholar 

  78. Nicolini F, Beghi C, Muscari C, Agostinelli A, Maria Budillon A, Spaggiari I, Gherli T (2003) Myocardial protection in adult cardiac surgery: current options and future challenges. Eur J Cardiothorac Surg 24:986–993

    PubMed  Google Scholar 

  79. Nogueira-Pedro A, Dias CC, Segreto HR, Addios PC, Lungato L, D’Almeida V, Barros CC, Higa EM, Buri MV, Paredes-Gamero EJ, Ferreira AT (2014) Nitric oxide-induced murine hematopoietic stem cell fate involves multiple signaling proteins, gene expression and redox modulation. Stem Cells 32:2949–2960

    CAS  PubMed  Google Scholar 

  80. O’Connor DM, O’Brien T (2009) Nitric oxide synthase gene therapy: progress and prospects. Expert Opin Biol Ther 9:867–878

    PubMed  Google Scholar 

  81. Oh I, Ozaki K, Sato K, Meguro A, Tatara R, Hatanaka K, Nagai T, Muroi K, Ozawa K (2007) Interferon-gamma and NF-kappaB mediate nitric oxide production by mesenchymal stromal cells. Biochem Biophys Res Commun 355:956–962

    CAS  PubMed  Google Scholar 

  82. Orciani M, Trubiani O, Vignini A, Mattioli-Belmonte M, Di Primio R, Salvolini E (2009) Nitric oxide production during the osteogenic differentiation of human periodontal ligament mesenchymal stem cells. Acta Histochem 111:15–24

    CAS  PubMed  Google Scholar 

  83. Pasini A, Bonafè F, Govoni M, Guarnieri C, Morselli PG, Sharma HS, Caldarera CM, Muscari C, Giordano E (2013) Epigenetic signature of early cardiac regulatory genes in native human adipose-derived stem cells. Cell Biochem Biophys 67:255–262

    CAS  PubMed  Google Scholar 

  84. Pasquinelli G, Vinci MC, Gamberini C, Orrico C, Foroni L, Guarnieri C, Parenti A, Gargiulo M, Ledda F, Caldarera CM, Muscari C (2009) Architectural organization and functional features of early endothelial progenitor cells cultured in a hyaluronan-based polymer scaffold. Tissue Eng Part A 15:2751–2762

    CAS  PubMed  Google Scholar 

  85. Pellegrino D, Parisella ML (2010) Nitrite as a physiological source of nitric oxide and a signalling molecule in the regulation of the cardiovascular system in both mammalian and non-mammalian vertebrates. Recent Pat Cardiovasc Drug Discov 5:91–96

    CAS  PubMed  Google Scholar 

  86. Penna C, Perrelli MG, Karam JP, Angotti C, Muscari C, Montero-Menei CN, Pagliaro P (2013) Pharmacologically active microcarriers influence VEGF-A effects on mesenchymal stem cell survival. J Cell Mol Med 17:192–204

    PubMed Central  CAS  PubMed  Google Scholar 

  87. Qi Y, Jiang Q, Chen C, Cao Y, Qian L (2013) Circulating endothelial progenitor cells decrease in infants with bronchopulmonary dysplasia and increase after inhaled nitric oxide. PLoS One 8:e79060

    PubMed Central  CAS  PubMed  Google Scholar 

  88. Ragy M, Elbassuoni E (2012) The role of nitric oxide and L-type calcium channel blocker in the contractility of rabbit ileum in vitro. J Physiol Biochem 68:521–528

    CAS  PubMed  Google Scholar 

  89. Rando TA (2001) Role of nitric oxide in the pathogenesis of muscular dystrophies: a “two hit” hypothesis of the cause of muscle necrosis. Microsc Res Tech 55:223–235

    CAS  PubMed  Google Scholar 

  90. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2:141–150

    CAS  PubMed  Google Scholar 

  91. Reynaert NL, Ckless K, Korn SH, Vos N, Guala AS, Wouters EF, van der Vliet A, Janssen-Heininger YM (2004) Nitric oxide represses inhibitory kappaB kinase through S-nitrosylation. Proc Natl Acad Sci U S A 101:8945–8950

    PubMed Central  CAS  PubMed  Google Scholar 

  92. Russwurm M, Behrends S, Harteneck C, Koesling D (1998) Functional properties of a naturally occurring isoform of soluble guanylyl cyclase. Biochem J 335(Pt 1):125–130

    PubMed Central  CAS  PubMed  Google Scholar 

  93. Sarti P, Arese M, Forte E, Giuffrè A, Mastronicola D (2012) Mitochondria and nitric oxide: chemistry and pathophysiology. Adv Exp Med Biol 942:75–92

    CAS  PubMed  Google Scholar 

  94. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K (2007) Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109:228–234

    CAS  PubMed  Google Scholar 

  95. Song H, Song BW, Cha MJ, Choi IG, Hwang KC (2010) Modification of mesenchymal stem cells for cardiac regeneration. Expert Opin Biol Ther 10:309–319

    PubMed  Google Scholar 

  96. Stefanelli C, Pignatti C, Tantini B, Stanic I, Bonavita F, Muscari C, Guarnieri C, Clo C, Caldarera CM (1999) Nitric oxide can function as either a killer molecule or an antiapoptotic effector in cardiomyocytes. Biochim Biophys Acta 1450:406–413

    CAS  PubMed  Google Scholar 

  97. Taylor EL, Li JT, Tupper JC, Rossi AG, Winn RK, Harlan JM (2007) GEA 3162, a peroxynitrite donor, induces Bcl-2-sensitive, p53-independent apoptosis in murine bone marrow cells. Biochem Pharmacol 74:1039–1049

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, Hussain P, Vecoli C, Paolocci N, Ambs S, Colton CA, Harris CC, Roberts DD, Wink DA (2008) The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 45:18–31

    PubMed Central  CAS  PubMed  Google Scholar 

  99. Tiribuzi R, Crispoltoni L, Tartacca F, Orlacchio A, Martino S, Palmerini CA, Orlacchio A (2013) Nitric oxide depletion alters hematopoietic stem cell commitment toward immunogenic dendritic cells. Biochim Biophys Acta 1830:2830–2838

    CAS  PubMed  Google Scholar 

  100. Tjabringa GS, Vezeridis PS, Zandieh-Doulabi B, Helder MN, Wuisman PI, Klein-Nulend J (2006) Polyamines modulate nitric oxide production and COX-2 gene expression in response to mechanical loading in human adipose tissue-derived mesenchymal stem cells. Stem Cells 24:2262–2269

    CAS  PubMed  Google Scholar 

  101. Tong J, Ding J, Shen X, Chen L, Bian Y, Ma G, Yao Y, Yang F (2013) Mesenchymal stem cell transplantation enhancement in myocardial infarction rat model under ultrasound combined with nitric oxide microbubbles. PLoS One 8:e80186

    PubMed Central  PubMed  Google Scholar 

  102. Tousoulis D, Kampoli AM, Tentolouris C, Papageorgiou N, Stefanadis C (2012) The role of nitric oxide on endothelial function. Curr Vasc Pharmacol 10:4–18

    CAS  PubMed  Google Scholar 

  103. Uezumi A, Ito T, Morikawa D, Shimizu N, Yoneda T, Segawa M, Yamaguchi M, Ogawa R, Matev MM, Miyagoe-Suzuki Y, Takeda S, Tsujikawa K, Tsuchida K, Yamamoto H, Fukada S (2011) Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. J Cell Sci 124:3654–3664

    CAS  PubMed  Google Scholar 

  104. Wang Y, Crisostomo PR, Wang M, Weil B, Abarbanell A, Poynter J, Manukyan MC, Meldrum DR (2008) Nitric oxide suppresses the secretion of vascular endothelial growth factor and hepatocyte growth factor from human mesenchymal stem cells. Shock 30:527–531

    PubMed  Google Scholar 

  105. Wong JC, Fiscus RR (2011) Essential roles of the nitric oxide (NO)/cGMP/protein kinase G type-Iα (PKG-Iα) signaling pathway and the atrial natriuretic peptide (ANP)/cGMP/PKG-Iα autocrine loop in promoting proliferation and cell survival of OP9 bone marrow stromal cells. J Cell Biochem 112:829–839

    CAS  PubMed  Google Scholar 

  106. Wozniak AC, Kong J, Bock E, Pilipowicz O, Anderson JE (2005) Signaling satellite-cell activation in skeletal muscle: markers, models, stretch, and potential alternate pathways. Muscle Nerve 31:283–300

    CAS  PubMed  Google Scholar 

  107. Yan K, Zhang R, Chen L, Chen F, Liu Y, Peng L, Sun H, Huang W, Sun C, Lv B, Li F, Cai Y, Tang Y, Zou Y, Du M, Qin L, Zhang H, Jiang X (2014) Nitric oxide-mediated immunosuppressive effect of human amniotic membrane-derived mesenchymal stem cells on the viability and migration of microglia. Brain Res. doi:10.1016/j.brainres.2014.05.041

    Google Scholar 

  108. Yiu KH, Tse HF (2014) Specific role of impaired glucose metabolism and diabetes mellitus in endothelial progenitor cell characteristics and function. Arterioscler Thromb Vasc Biol 34:1136–1143

    CAS  PubMed  Google Scholar 

  109. Yoshida K, Kita Y (2005) Hydroxyimine NO-donors; FK409 and derivatives. Curr Top Med Chem 5:675–685

    CAS  PubMed  Google Scholar 

  110. Zanella B, Giordano E, Muscari C, Zini M, Guarnieri C (2004) Nitric oxide synthase activity in rat cardiac mitochondria. Basic Res Cardiol 99:159–164

    CAS  PubMed  Google Scholar 

  111. Zhang L, Dang RJ, Li H, Li P, Yang YM, Guo XM, Wang XY, Fang NZ, Mao N, Wen N, Jiang XX (2014) SOCS1 regulates the immune modulatory properties of mesenchymal stem cells by inhibiting nitric oxide production. PLoS One 9:e97256

    PubMed Central  PubMed  Google Scholar 

  112. Zucchi R, Ghelardoni S, Evangelista S (2007) Biochemical basis of ischemic heart injury and of cardioprotective interventions. Curr Med Chem 14:1619–1637

    CAS  PubMed  Google Scholar 

  113. Zweier JL, Samouilov A, Kuppusamy P (1999) Non-enzymatic nitric oxide synthesis in biological systems. Biochim Biophys Acta 1411:250–262

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical and Neuromotor Sciences, University of Bologna, Via Irnerio, 48, 40126, Bologna, Italy

    Francesca Bonafè, Carlo Guarnieri & Claudio Muscari

Authors
  1. Francesca Bonafè
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlo Guarnieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudio Muscari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudio Muscari.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bonafè, F., Guarnieri, C. & Muscari, C. Nitric oxide regulates multiple functions and fate of adult progenitor and stem cells. J Physiol Biochem 71, 141–153 (2015). https://doi.org/10.1007/s13105-014-0373-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13105-014-0373-9

Keywords

Search

Navigation