Advertisement

Gasotransmitters: Antimicrobial Properties and Impact on Cell Growth for Tissue Engineering

  • Kenyatta S. Washington
  • Chris A. BashurEmail author
Chapter
  • 129 Downloads

Abstract

Several clinical situations including birth defects, trauma, and fracture nonunions often result in critical-sized defects that require a graft that can remodel and integrate with the existing bone as well as mitigate the risk of infectious complications. Delivery of gasotransmitters from tissue engineering scaffolds is a potential option to provide antibacterial properties while simultaneously promoting osteogenesis and tissue vascularization. Gasotransmitters, such as nitric oxide, carbon monoxide, and hydrogen sulfide, are inorganic gases that have an important role in cell signaling, and supplemental doses have also been shown to provide bactericidal properties. This chapter reviews the importance of understanding the complex and dose-dependent impacts of different gasotransmitters on both bacterial and mammalian cells. The current research into the selectivity of a gasotransmitter dose for killing bacterial cells compared to mammalian cells is a particular focus. The chapter also discusses the applications of gasotransmitters to engineered tissues, with a focus on bone and microvasculature, as well as the current limitations for incorporating gasotransmitters within scaffolds that need to be addressed.

Keywords

Gasotransmitters Antimicrobial agents Tissue engineering Scaffolds Bone regeneration Carbon monoxide Nitric oxide Hydrogen sulfide Tissue vascularization Drug delivery 

Notes

Acknowledgment

Funding: Efforts were supported by the National Science Foundation under Grant No. CBET 1510003.

References

  1. 1.
    Damoulis PD, Drakos DE, Gagari E, Kaplan DL (2007) Osteogenic differentiation of human mesenchymal bone marrow cells in silk scaffolds is regulated by nitric oxide. Ann N Y Acad Sci 1117:367–376.  https://doi.org/10.1196/annals.1402.038. NIH Public AccessCrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Nichols SP, Storm WL, Koh A, Schoenfisch MH (2012) Local delivery of nitric oxide: targeted delivery of therapeutics to bone and connective tissues. Adv Drug Deliv Rev 64(12):1177–1188.  https://doi.org/10.1016/J.ADDR.2012.03.002. ElsevierCrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Pant J, Sundaram J, Goudie MJ, Nguyen DT, Handa H (2018) Antibacterial 3D bone scaffolds for tissue engineering application. J Biomed Mater Res B Appl Biomater 107:1068–1078.  https://doi.org/10.1002/jbm.b.34199CrossRefPubMedGoogle Scholar
  4. 4.
    Einhorn TA, Lee CA (2001) Bone regeneration: new findings and potential clinical applications. J Am Acad Orthop Surg 9(3):157–165.  https://doi.org/10.5435/00124635-200105000-00002CrossRefPubMedGoogle Scholar
  5. 5.
    Keramaris NC, Calori GM, Nikolaou VS, Schemitsch EH, Giannoudis PV (2008) Fracture vascularity and bone healing: a systematic review of the role of VEGF. Injury 39(Suppl 2):S45–S57.  https://doi.org/10.1016/S0020-1383(08)70015-9. ElsevierCrossRefPubMedGoogle Scholar
  6. 6.
    Darouiche RO (2003) Antimicrobial approaches for preventing infections associated with surgical implants. Clin Infect Dis 36(10):1284–1289.  https://doi.org/10.1086/374842CrossRefPubMedGoogle Scholar
  7. 7.
    Dentino A, Lee S, Mailhot J, Hefti AF (2013) Principles of periodontology. Periodontology 2000 61(1):16–53.  https://doi.org/10.1111/j.1600-0757.2011.00397.x. WileyCrossRefPubMedGoogle Scholar
  8. 8.
    Thomas MV, Puleo DA (2011) Infection, inflammation, and bone regeneration: a paradoxical relationship. J Dent Res 90(9):1052–1061.  https://doi.org/10.1177/0022034510393967. International Association for Dental ResearchCrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Johnson CT, García AJ (2015) Scaffold-based anti-infection strategies in bone repair. Ann Biomed Eng 43(3):515–528.  https://doi.org/10.1007/s10439-014-1205-3. NIH Public AccessCrossRefPubMedGoogle Scholar
  10. 10.
    Mortimer CJ, Widdowson JP, Wright CJ (2018) Electrospinning of functional nanofibers for regenerative medicine: from bench to commercial scale. In: Novel aspects of nanofibers. InTech.  https://doi.org/10.5772/intechopen.73677Google Scholar
  11. 11.
    Daghighi S, Sjollema J, van der Mei HC, Busscher HJ, Rochford ETJ (2013) Infection resistance of degradable versus non-degradable biomaterials: an assessment of the potential mechanisms. Biomaterials 34(33):8013–8017.  https://doi.org/10.1016/J.BIOMATERIALS.2013.07.044. ElsevierCrossRefPubMedGoogle Scholar
  12. 12.
    Kim J, Li WA, Sands W, Mooney DJ (2014) Effect of pore structure of macroporous poly(lactide-co-glycolide) scaffolds on the in vivo enrichment of dendritic cells. ACS Appl Mater Interfaces 6(11):8505–8512.  https://doi.org/10.1021/am501376n. American Chemical SocietyCrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Klein-Nulend J, van Oers RFM, Bakker AD, Bacabac RG (2013) Nitric oxide signaling in mechanical adaptation of bone. Osteoporos Int 25(5):1427–1437.  https://doi.org/10.1007/s00198-013-2590-4CrossRefPubMedGoogle Scholar
  14. 14.
    Chinta KC, Saini V, Glasgow JN, Mazorodze JH, Rahman MA, Reddy D, Lancaster JR, Steyn AJC, Steyn AJC (2016) The emerging role of gasotransmitters in the pathogenesis of tuberculosis. Nitric Oxide 59:28–41.  https://doi.org/10.1016/j.niox.2016.06.009. NIH Public AccessCrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Fang FC (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2(10):820–832.  https://doi.org/10.1038/nrmicro1004CrossRefPubMedGoogle Scholar
  16. 16.
    Arkenau H-T, Stichtenoth DO, Frölich JC, Manns MP, Böker K-HW (2002) Elevated nitric oxide levels in patients with chronic liver disease and cirrhosis correlate with disease stage and parameters of hyperdynamic circulation. Z Gastroenterol 40(11):907–913.  https://doi.org/10.1055/s-2002-35413. © Karl Demeter Verlag im Georg Thieme Verlag Stuttgart, New YorkCrossRefPubMedGoogle Scholar
  17. 17.
    Wimalawansa SJ (2010) Nitric oxide and bone. Ann N Y Acad Sci 1192(1):391–403.  https://doi.org/10.1111/j.1749-6632.2009.05230.xCrossRefPubMedGoogle Scholar
  18. 18.
    Wimalawansa SJ (2008) Nitric oxide: novel therapy for osteoporosis. Expert Opin Pharmacother 9(17):3025–3044.  https://doi.org/10.1517/14656560802197162CrossRefPubMedGoogle Scholar
  19. 19.
    Pryor WA, Squadrito GL (1995) The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol 268(5 Pt 1):L699–L722.  https://doi.org/10.1152/ajplung.1995.268.5.L699. American Physiological Society, Bethesda, MDCrossRefPubMedGoogle Scholar
  20. 20.
    Carter JM, Qian Y, Foster JC, Matson JB (2015) Peptide-based hydrogen sulphide-releasing gels. Chem Commun 51(66):13131–13134.  https://doi.org/10.1039/C5CC04883D. Royal Society of ChemistryCrossRefGoogle Scholar
  21. 21.
    George TJ, Arnaoutakis GJ, Beaty CA, Jandu SK, Santhanam L, Berkowitz DE, Shah AS (2012) Inhaled hydrogen sulfide improves graft function in an experimental model of lung transplantation. J Surg Res 178(2):593–600.  https://doi.org/10.1016/j.jss.2012.06.037. NIH Public AccessCrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Pu H, Hua Y (2017) Hydrogen sulfide regulates bone remodeling and promotes orthodontic tooth movement. Mol Med Rep 16(6):9415–9422.  https://doi.org/10.3892/mmr.2017.7813. Spandidos PublicationsCrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Zhang L, Wang Y, Li Y, Li L, Xu S, Feng X, Liu S (2018) Hydrogen sulfide (H2S)-releasing compounds: therapeutic potential in cardiovascular diseases. Front Pharmacol 9:1066.  https://doi.org/10.3389/fphar.2018.01066. Frontiers Media SACrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Bhatia M (2005) Hydrogen sulfide as a vasodilator. IUBMB Life 57(9):603–606.  https://doi.org/10.1080/15216540500217875. WileyCrossRefPubMedGoogle Scholar
  25. 25.
    Kimura H (2002) Hydrogen sulfide as a neuromodulator. Mol Neurobiol 26(1):013–020.  https://doi.org/10.1385/MN:26:1:013. Humana PressCrossRefGoogle Scholar
  26. 26.
    Łowicka E, Bełtowski J (2007) Hydrogen sulfide (H2S)—the third gas of interest for pharmacologists. Pharmacol Rep 59(1):4–24. http://www.ncbi.nlm.nih.gov/pubmed/17377202PubMedGoogle Scholar
  27. 27.
    Wang R (2003) The gasotransmitter role of hydrogen sulfide. Antioxid Redox Signal 5(4):493–501.  https://doi.org/10.1089/152308603768295249. Mary Ann Liebert, Inc.CrossRefPubMedGoogle Scholar
  28. 28.
    WANG RUI (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16(13):1792–1798.  https://doi.org/10.1096/fj.02-0211hyp. Federation of American Societies for Experimental BiologyCrossRefPubMedGoogle Scholar
  29. 29.
    Gadalla MM, Snyder SH (2010) Hydrogen sulfide as a gasotransmitter. J Neurochem 113(1):14–26.  https://doi.org/10.1111/j.1471-4159.2010.06580.x. NIH Public AccessCrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Pal VK, Bandyopadhyay P, Singh A (2018) Hydrogen sulfide in physiology and pathogenesis of bacteria and viruses. IUBMB Life 70(5):393–410.  https://doi.org/10.1002/iub.1740. Europe PMC FundersCrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Wegiel B, Gallo DJ, Raman KG, Karlsson JM, Ozanich B, Chin BY, Tzeng E et al (2010) Nitric oxide–dependent bone marrow progenitor mobilization by carbon monoxide enhances endothelial repair after vascular injury. Circulation 121(4):537–548.  https://doi.org/10.1161/CIRCULATIONAHA.109.887695CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Babu D, Motterlini R, Lefebvre RA (2015) CO and CO-releasing molecules (CO-RMs) in acute gastrointestinal inflammation. Br J Pharmacol 172(6):1557–1573.  https://doi.org/10.1111/bph.12632CrossRefPubMedGoogle Scholar
  33. 33.
    Ahmed A, Ramma W (2015) Unravelling the theories of pre-eclampsia: are the protective pathways the new paradigm? Br J Pharmacol 172(6):1574–1586.  https://doi.org/10.1111/bph.12977CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Washington KS, Bashur CA (2017) Delivery of antioxidant and anti-inflammatory agents for tissue engineered vascular grafts. Front Pharmacol 8:659.  https://doi.org/10.3389/fphar.2017.00659. FrontiersCrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Nobre LS, Jeremias H, Romão CC, Saraiva LM, Schenk WA, Benz R, Zimmermann U et al (2016) Examining the antimicrobial activity and toxicity to animal cells of different types of CO-releasing molecules. Dalton Trans 45(4):1455–1466.  https://doi.org/10.1039/C5DT02238J. The Royal Society of ChemistryCrossRefPubMedGoogle Scholar
  36. 36.
    Wilson JL, Jesse HE, Hughes B, Lund V, Naylor K, Davidge KS, Cook GM, Mann BE, Poole RK (2013) Ru(CO)3 Cl(glycinate) (CORM-3): a carbon monoxide–releasing molecule with broad-spectrum antimicrobial and photosensitive activities against respiration and cation transport in Escherichia Coli. Antioxid Redox Signal 19(5):497–509.  https://doi.org/10.1089/ars.2012.4784CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Desmard M, Foresti R, Morin D, Dagouassat M, Berdeaux A, Denamur E, Crook SH et al (2012) Differential antibacterial activity against Pseudomonas aeruginosa by carbon monoxide-releasing molecules. Antioxid Redox Signal 16(2):153–163.  https://doi.org/10.1089/ars.2011.3959CrossRefPubMedGoogle Scholar
  38. 38.
    Deupree SM, Schoenfisch MH (2009) Morphological analysis of the antimicrobial action of nitric oxide on gram-negative pathogens using atomic force microscopy. Acta Biomater 5(5):1405–1415.  https://doi.org/10.1016/J.ACTBIO.2009.01.025. ElsevierCrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Shatalin K, Gusarov I, Avetissova E, Shatalina Y, McQuade LE, Lippard SJ, Nudler E (2008) Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc Natl Acad Sci 105(3):1009–1013.  https://doi.org/10.1073/pnas.0710950105CrossRefPubMedGoogle Scholar
  40. 40.
    Ghaffari A, Neil DH, Ardakani A, Road J, Ghahary A, Miller CC (2005) A direct nitric oxide gas delivery system for bacterial and mammalian cell cultures. Nitric Oxide 12(3):129–140.  https://doi.org/10.1016/J.NIOX.2005.01.006. AcademicCrossRefPubMedGoogle Scholar
  41. 41.
    Shim JS, Park D-s, Baek D-H, Jha N, In Park S, Yun HJ, Kim WJ, Ryu JJ (2018) Antimicrobial activity of NO-releasing compounds against periodontal pathogens. PLoS One 13(10):e0199998.  https://doi.org/10.1371/journal.pone.0199998. Edited by Salomon Amar. Public Library of ScienceCrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Shatalin K, Shatalina E, Mironov A, Nudler E (2011) H2S: a universal defense against antibiotics in bacteria. Science 334(6058):986–990.  https://doi.org/10.1126/science.1209855CrossRefPubMedGoogle Scholar
  43. 43.
    Wu D, Li M, Tian W, Wang S, Cui L, Li H, Wang H, Ji A, Li Y (2017) Hydrogen sulfide acts as a double-edged sword in human hepatocellular carcinoma cells through EGFR/ERK/MMP-2 and PTEN/AKT signaling pathways. Sci Rep 7(1):5134.  https://doi.org/10.1038/s41598-017-05457-z. Nature Publishing GroupCrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Fu L-H, Wei Z-Z, Hu K-D, Hu L-Y, Li Y-H, Chen X-Y, Han Z, Yao G-F, Zhang H (2018) Hydrogen sulfide inhibits the growth of Escherichia coli through oxidative damage. J Microbiol 56(4):238–245.  https://doi.org/10.1007/s12275-018-7537-1. The Microbiological Society of KoreaCrossRefPubMedGoogle Scholar
  45. 45.
    Motterlini R, Otterbein LE (2010) The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 9(9):728–743.  https://doi.org/10.1038/nrd3228CrossRefPubMedGoogle Scholar
  46. 46.
    Tinajero-Trejo M, Jesse HE, Poole RK (2013) Gasotransmitters, poisons, and antimicrobials: it’s a gas, gas, gas! F1000Prime Rep 5:28.  https://doi.org/10.12703/P5-28. Faculty of 1000 LtdCrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Slonczewski J, Foster JW (2009) Microbiology: an evolving science, 1st edn. W.W. Norton & Co, New York. https://www.worldcat.org/title/microbiology-an-evolving-science/oclc/185042615Google Scholar
  48. 48.
    Arruebarrena Di Palma A, Pereyra CM, Moreno Ramirez L, Xiqui Vázquez ML, Baca BE, Pereyra MA, Lamattina L, Creus CM (2013) Denitrification-derived nitric oxide modulates biofilm formation in Azospirillum brasilense. FEMS Microbiol Lett 338(1):77–85.  https://doi.org/10.1111/1574-6968.12030CrossRefPubMedGoogle Scholar
  49. 49.
    Barnes RJ, Bandi RR, Wong WS, Barraud N, McDougald D, Fane A, Kjelleberg S, Rice SA (2013) Optimal dosing regimen of nitric oxide donor compounds for the reduction of Pseudomonas aeruginosa biofilm and isolates from wastewater membranes. Biofouling 29(2):203–212.  https://doi.org/10.1080/08927014.2012.760069CrossRefPubMedGoogle Scholar
  50. 50.
    Gusarov I, Nudler E (2005) NO-mediated cytoprotection: instant adaptation to oxidative stress in bacteria. Proc Natl Acad Sci 102(39):13855–13860.  https://doi.org/10.1073/pnas.0504307102CrossRefPubMedGoogle Scholar
  51. 51.
    Gardner PR, Gardner AM, Martin LA, Salzman AL (1998) Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc Natl Acad Sci U S A 95(18):10378–10383. http://www.ncbi.nlm.nih.gov/pubmed/9724711CrossRefGoogle Scholar
  52. 52.
    Wisecaver JH, Alexander WG, King SB, Todd Hittinger C, Rokas A (2016) Dynamic evolution of nitric oxide detoxifying flavohemoglobins, a family of single-protein metabolic modules in bacteria and eukaryotes. Mol Biol Evol 33(8):1979–1987.  https://doi.org/10.1093/molbev/msw073CrossRefPubMedGoogle Scholar
  53. 53.
    Laver JR, McLean S, Bowman LAH, Harrison LJ, Read RC, Poole RK (2013) Nitrosothiols in bacterial pathogens and pathogenesis. Antioxid Redox Signal 18(3):309–322.  https://doi.org/10.1089/ars.2012.4767CrossRefPubMedGoogle Scholar
  54. 54.
    Gusarov I, Shatalin K, Starodubtseva M, Nudler E (2009) Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325(5946):1380–1384.  https://doi.org/10.1126/science.1175439CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Nakahira K, Choi AMK (2015) Carbon monoxide in the treatment of sepsis. Am J Physiol Lung Cell Mol Physiol 309(12):L1387–L1393.  https://doi.org/10.1152/ajplung.00311.2015. American Physiological SocietyCrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Nilforoushan D, Gramoun A, Glogauer M, Manolson MF (2009) Nitric oxide enhances osteoclastogenesis possibly by mediating cell fusion. Nitric Oxide 21(1):27–36.  https://doi.org/10.1016/J.NIOX.2009.04.002. AcademicCrossRefPubMedGoogle Scholar
  57. 57.
    Mancini L, Moradi-Bidhendi N, Becherini L, Martineti V, MacIntyre I (2000) The biphasic effects of nitric oxide in primary rat osteoblasts are CGMP dependent. Biochem Biophys Res Commun 274(2):477–481.  https://doi.org/10.1006/bbrc.2000.3164CrossRefPubMedGoogle Scholar
  58. 58.
    Holliday LS, Dean AD, Lin RH, Greenwald JE, Gluck SL (1997) Low NO concentrations inhibit osteoclast formation in mouse marrow cultures by CGMP-dependent mechanism. Am J Physiol 272(3):F283–F291.  https://doi.org/10.1152/ajprenal.1997.272.3.F283CrossRefPubMedGoogle Scholar
  59. 59.
    Guo F-F, Yu T-C, Hong J, Fang J-Y (2016) Emerging roles of hydrogen sulfide in inflammatory and neoplastic colonic diseases. Front Physiol 7:156.  https://doi.org/10.3389/fphys.2016.00156. Frontiers Media SACrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Cai W-J, Wang M-J, Ju L-H, Wang C, Zhu Y-C (2010) Hydrogen sulfide induces human colon cancer cell proliferation: role of Akt, ERK and P21. Cell Biol Int 34(6):565–572.  https://doi.org/10.1042/CBI20090368CrossRefPubMedGoogle Scholar
  61. 61.
    Krischel V, Bruch-Gerharz D, Suschek C, Kröncke K-D, Ruzicka T, Kolb-Bachofen V (1998) Biphasic effect of exogenous nitric oxide on proliferation and differentiation in skin derived keratinocytes but not fibroblasts. J Investig Dermatol 111(2):286–291.  https://doi.org/10.1046/j.1523-1747.1998.00268.xCrossRefPubMedGoogle Scholar
  62. 62.
    Lowson SM (2004) Alternatives to nitric oxide. Br Med Bull 70:119–131.  https://doi.org/10.1093/bmb/ldh028CrossRefPubMedGoogle Scholar
  63. 63.
    Ziesche S, Franciosa JA (1977) Clinical application of sodium nitroprusside. Heart Lung 6(1):99–103. http://www.ncbi.nlm.nih.gov/pubmed/583902PubMedGoogle Scholar
  64. 64.
    Gregory EK, Vavra AK, Moreira ES, Havelka GE, Jiang Q, Lee VR, Van Lith R, Ameer GA, Kibbe MR (2011) Antioxidants modulate the antiproliferative effects of nitric oxide on vascular smooth muscle cells and adventitial fibroblasts by regulating oxidative stress. Am J Surg 202(5):536–540.  https://doi.org/10.1016/j.amjsurg.2011.06.018CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Elnaggar MA, Seo SH, Gobaa S, Lim KS, Bae I-H, Jeong MH, Han DK, Joung YK (2016) Nitric oxide releasing coronary stent: a new approach using layer-by-layer coating and liposomal encapsulation. Small 12(43):6012–6023.  https://doi.org/10.1002/smll.201600337CrossRefPubMedGoogle Scholar
  66. 66.
    Jones ML, Ganopolsky JG, Labbé A, Prakash S (2010) A novel nitric oxide producing probiotic patch and its antimicrobial efficacy: preparation and in vitro analysis. Appl Microbiol Biotechnol 87(2):509–516.  https://doi.org/10.1007/s00253-010-2490-xCrossRefPubMedGoogle Scholar
  67. 67.
    Lowe A, Bills J, Verma R, Lavery L, Davis K, Balkus KJ (2015) Electrospun nitric oxide releasing bandage with enhanced wound healing. Acta Biomater 13:121–130.  https://doi.org/10.1016/J.ACTBIO.2014.11.032. ElsevierCrossRefPubMedGoogle Scholar
  68. 68.
    Frank S, Kämpfer H, Wetzler C, Pfeilschifter J (2002) Nitric oxide drives skin repair: novel functions of an established mediator. Kidney Int 61(3):882–888.  https://doi.org/10.1046/J.1523-1755.2002.00237.X. ElsevierCrossRefPubMedGoogle Scholar
  69. 69.
    Joseph CA, McCarthy CW, Tyo AG, Hubbard KR, Fisher HC, Altscheffel JA, He W et al (2019) Development of an injectable nitric oxide releasing poly(ethylene) glycol-fibrin adhesive hydrogel. ACS Biomater Sci Eng 5(2):959–969.  https://doi.org/10.1021/acsbiomaterials.8b01331. American Chemical SocietyCrossRefPubMedGoogle Scholar
  70. 70.
    Wan X, Wang Y, Jin X, Li P, Yuan J, Shen J (2018) Heparinized PCL/keratin mats for vascular tissue engineering scaffold with potential of catalytic nitric oxide generation. J Biomater Sci Polym Ed 29(14):1785–1798.  https://doi.org/10.1080/09205063.2018.1504192. Taylor & FrancisCrossRefPubMedGoogle Scholar
  71. 71.
    Feng S, Zhao Y, Xian M, Wang Q (2015) Biological thiols-triggered hydrogen sulfide releasing microfibers for tissue engineering applications. Acta Biomater 27:205–213.  https://doi.org/10.1016/j.actbio.2015.09.010. NIH Public AccessCrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Raggio R, Bonani W, Callone E, Dirè S, Gambari L, Grassi F, Motta A (2018) Silk fibroin porous scaffolds loaded with a slow-releasing hydrogen sulfide agent (GYY4137) for applications of tissue engineering. ACS Biomater Sci Eng 4(8):2956–2966.  https://doi.org/10.1021/acsbiomaterials.8b00212. American Chemical SocietyCrossRefGoogle Scholar
  73. 73.
    Lee ZW, Zhou J, Chen C-S, Zhao Y, Tan C-H, Li L, Moore PK, Deng L-W (2011) The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLoS One 6(6):e21077.  https://doi.org/10.1371/journal.pone.0021077. Edited by Joseph Alan Bauer. Public Library of ScienceCrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Bohlender C, Gläser S, Klein M, Weisser J, Thein S, Neugebauer U, Popp J, Wyrwa R, Schiller A (2014) Light-triggered CO release from nanoporous non-wovens. J Mater Chem B 2(11):1454–1463.  https://doi.org/10.1039/C3TB21649G. Royal Society of ChemistryCrossRefGoogle Scholar
  75. 75.
    Michael E, Abeyrathna N, Patel AV, Liao Y, Bashur CA (2016) Incorporation of photo-carbon monoxide releasing materials into electrospun scaffolds for vascular tissue engineering. Biomed Mater (Bristol, England) 11(2):025009.  https://doi.org/10.1088/1748-6041/11/2/025009CrossRefGoogle Scholar
  76. 76.
    Rajfer RA, Kilic A, Neviaser AS, Schulte LM, Hlaing SM, Landeros J, Ferrini MG, Ebramzadeh E, Park S-H (2017) Enhancement of fracture healing in the rat, modulated by compounds that stimulate inducible nitric oxide synthase: acceleration of fracture healing via inducible nitric oxide synthase. Bone Joint Res 6(2):90–97.  https://doi.org/10.1302/2046-3758.62.BJR-2016-0164.R2. British Editorial Society of Bone and Joint SurgeryCrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Lin S-K, Kok S-H, Kuo MY-P, Lee M-S, Wang C-C, Lan W-H, Hsiao M, Goldring SR, Hong C-Y (2003) Nitric oxide promotes infectious bone resorption by enhancing cytokine-stimulated interstitial collagenase synthesis in osteoblasts. J Bone Miner Res 18(1):39–46.  https://doi.org/10.1359/jbmr.2003.18.1.39CrossRefPubMedGoogle Scholar
  78. 78.
    Zheng Y, Liao F, Lin X, Zheng F, Fan J, Cui Q, Yang J, Geng B, Cai J (2017) Cystathionine γ-lyase-hydrogen sulfide induces runt-related transcription factor 2 sulfhydration, thereby increasing osteoblast activity to promote bone fracture healing. Antioxid Redox Signal 27(11):742–753.  https://doi.org/10.1089/ars.2016.6826CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Hikiji H, Shin WS, Oida S, Takato T, Koizumi T, Toyo-oka T (1997) Direct action of nitric oxide on osteoblastic differentiation. FEBS Lett 410(2–3):238–242.  https://doi.org/10.1016/S0014-5793(97)00597-8. No longer published by ElsevierCrossRefPubMedGoogle Scholar
  80. 80.
    Sonoda S, Mei Y-f, Atsuta I, Danjo A, Yamaza H, Hama S, Nishida K et al (2018) Exogenous nitric oxide stimulates the odontogenic differentiation of rat dental pulp stem cells. Sci Rep 8(1):3419.  https://doi.org/10.1038/s41598-018-21183-6. Nature Publishing GroupCrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Kalyanaraman H, Ramdani G, Joshua J, Schall N, Boss GR, Cory E, Sah RL, Casteel DE, Pilz RB (2017) A novel, direct NO donor regulates osteoblast and osteoclast functions and increases bone mass in ovariectomized mice. J Bone Miner Res 32(1):46–59.  https://doi.org/10.1002/jbmr.2909. WileyCrossRefPubMedGoogle Scholar
  82. 82.
    Xu Z-S, Wang X-Y, Xiao D-M, Hu L-F, Lu M, Wu Z-Y, Bian J-S (2011) Hydrogen sulfide protects MC3T3-E1 osteoblastic cells against H2O2-induced oxidative damage—implications for the treatment of osteoporosis. Free Radic Biol Med 50(10):1314–1323.  https://doi.org/10.1016/j.freeradbiomed.2011.02.016CrossRefPubMedGoogle Scholar
  83. 83.
    Grassi F, Tyagi AM, Calvert JW, Gambari L, Walker LD, Yu M, Robinson J et al (2016) Hydrogen sulfide is a novel regulator of bone formation implicated in the bone loss induced by estrogen deficiency. J Bone Miner Res 31(5):949–963.  https://doi.org/10.1002/jbmr.2757. NIH Public AccessCrossRefPubMedGoogle Scholar
  84. 84.
    Almubarak S, Nethercott H, Freeberg M, Beaudon C, Jha A, Jackson W, Marcucio R, Miclau T, Healy K, Bahney C (2016) Tissue engineering strategies for promoting vascularized bone regeneration. Bone 83:197–209.  https://doi.org/10.1016/j.bone.2015.11.011. NIH Public AccessCrossRefPubMedGoogle Scholar
  85. 85.
    Volti GL, Sacerdoti D, Sangras B, Vanella A, Mezentsev A, Scapagnini G, Falck JR, Abraham NG (2005) Carbon monoxide signaling in promoting angiogenesis in human microvessel endothelial cells. Antioxid Redox Signal 7(5–6):704–710.  https://doi.org/10.1089/ars.2005.7.704CrossRefGoogle Scholar
  86. 86.
    Ziche M, Morbidelli L, Masini E, Amerini S, Granger HJ, Maggi CA, Geppetti P, Ledda F (1994) Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 94(5):2036–2044.  https://doi.org/10.1172/JCI117557CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Priya MK, Sahu G, Soto-Pantoja DR, Goldy N, Sundaresan AM, Jadhav V, Barathkumar TR et al (2015) Tipping off endothelial tubes: nitric oxide drives tip cells. Angiogenesis 18(2):175–189.  https://doi.org/10.1007/s10456-014-9455-0CrossRefPubMedGoogle Scholar
  88. 88.
    Phillips PG, Birnby LM, Narendran A, Milonovich WL (2001) Nitric oxide modulates capillary formation at the endothelial cell-tumor cell interface. Am J Physiol Lung Cell Mol Physiol 281(1):L278–L290.  https://doi.org/10.1152/ajplung.2001.281.1.L278. American Physiological Society, Bethesda, MDCrossRefPubMedGoogle Scholar
  89. 89.
    Wang M-J, Cai W-J, Zhu Y-C (2010) Mechanisms of angiogenesis: role of hydrogen sulphide. Clin Exp Pharmacol Physiol 37(7):764–771.  https://doi.org/10.1111/j.1440-1681.2010.05371.x. WileyCrossRefPubMedGoogle Scholar
  90. 90.
    Shantz S, Alan J, Yu Y-Y, Andres W, Miclau T, Marcucio R (2014) Modulation of macrophage activity during fracture repair has differential effects in young adult and elderly mice. J Orthop Trauma 28:S10–S14.  https://doi.org/10.1097/BOT.0000000000000062CrossRefGoogle Scholar
  91. 91.
    Xing Z, Lu C, Hu D, Yu Y-y, Wang X, Colnot C, Nakamura M, Wu Y, Miclau T, Marcucio RS (2010) Multiple roles for CCR2 during fracture healing. Dis Model Mech 3(7–8):451–458.  https://doi.org/10.1242/dmm.003186CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biomedical and Chemical Engineering and SciencesFlorida Institute of TechnologyMelbourneUSA

Personalised recommendations