Skip to main content
SpringerLink
Log in

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

  • Chapter
  • First Online:
Racing for the Surface

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.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  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 Access

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Elsevier

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.34199

    Article  CAS  PubMed  Google Scholar 

  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/10.5435/00124635-200105000-00002

    Article  CAS  PubMed  Google Scholar 

  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. Elsevier

    Article  PubMed  Google Scholar 

  6. Darouiche RO (2003) Antimicrobial approaches for preventing infections associated with surgical implants. Clin Infect Dis 36(10):1284–1289. https://doi.org/10.1086/374842

    Article  PubMed  Google Scholar 

  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. Wiley

    Article  PubMed  Google Scholar 

  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 Research

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Access

    Article  PubMed  Google Scholar 

  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.73677

    Google Scholar 

  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. Elsevier

    Article  CAS  PubMed  Google Scholar 

  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 Society

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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/s00198-013-2590-4

    Article  CAS  PubMed  Google Scholar 

  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 Access

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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/nrmicro1004

    Article  CAS  PubMed  Google Scholar 

  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 York

    Article  CAS  PubMed  Google Scholar 

  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.x

    Article  CAS  PubMed  Google Scholar 

  18. Wimalawansa SJ (2008) Nitric oxide: novel therapy for osteoporosis. Expert Opin Pharmacother 9(17):3025–3044. https://doi.org/10.1517/14656560802197162

    Article  CAS  PubMed  Google Scholar 

  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, MD

    Article  CAS  PubMed  Google Scholar 

  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 Chemistry

    Article  CAS  Google Scholar 

  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 Access

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Publications

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 SA

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bhatia M (2005) Hydrogen sulfide as a vasodilator. IUBMB Life 57(9):603–606. https://doi.org/10.1080/15216540500217875. Wiley

    Article  CAS  PubMed  Google Scholar 

  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 Press

    Article  CAS  Google Scholar 

  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/17377202

    PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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 Biology

    Article  CAS  PubMed  Google Scholar 

  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 Access

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Funders

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.109.887695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.12632

    Article  CAS  PubMed  Google Scholar 

  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.12977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Frontiers

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Chemistry

    Article  CAS  PubMed  Google Scholar 

  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.2012.4784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.2011.3959

    Article  CAS  PubMed  Google Scholar 

  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. Elsevier

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.0710950105

    Article  CAS  PubMed  Google Scholar 

  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. Academic

    Article  CAS  PubMed  Google Scholar 

  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 Science

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.1209855

    Article  CAS  PubMed  Google Scholar 

  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 Group

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Korea

    Article  CAS  PubMed  Google Scholar 

  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/nrd3228

    Article  CAS  PubMed  Google Scholar 

  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 Ltd

    Article  PubMed  PubMed Central  Google Scholar 

  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/185042615

    Google Scholar 

  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/10.1111/1574-6968.12030

    Article  CAS  PubMed  Google Scholar 

  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/10.1080/08927014.2012.760069

    Article  CAS  PubMed  Google Scholar 

  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.0504307102

    Article  CAS  PubMed  Google Scholar 

  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/9724711

    Article  CAS  Google Scholar 

  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/msw073

    Article  CAS  PubMed  Google Scholar 

  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.2012.4767

    Article  CAS  PubMed  Google Scholar 

  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.1175439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Society

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Academic

    Article  CAS  PubMed  Google Scholar 

  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.2000.3164

    Article  CAS  PubMed  Google Scholar 

  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.F283

    Article  CAS  PubMed  Google Scholar 

  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 SA

    Article  PubMed  PubMed Central  Google Scholar 

  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/CBI20090368

    Article  CAS  PubMed  Google Scholar 

  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.x

    Article  CAS  PubMed  Google Scholar 

  62. Lowson SM (2004) Alternatives to nitric oxide. Br Med Bull 70:119–131. https://doi.org/10.1093/bmb/ldh028

    Article  CAS  PubMed  Google Scholar 

  63. Ziesche S, Franciosa JA (1977) Clinical application of sodium nitroprusside. Heart Lung 6(1):99–103. http://www.ncbi.nlm.nih.gov/pubmed/583902

    CAS  PubMed  Google Scholar 

  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.2011.06.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.201600337

    Article  CAS  PubMed  Google Scholar 

  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-x

    Article  CAS  PubMed  Google Scholar 

  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. Elsevier

    Article  CAS  PubMed  Google Scholar 

  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. Elsevier

    Article  CAS  PubMed  Google Scholar 

  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 Society

    Article  CAS  PubMed  Google Scholar 

  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 & Francis

    Article  CAS  PubMed  Google Scholar 

  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 Access

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Society

    Article  CAS  Google Scholar 

  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 Science

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Chemistry

    Article  CAS  Google Scholar 

  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/10.1088/1748-6041/11/2/025009

    Article  CAS  Google Scholar 

  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 Surgery

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.2003.18.1.39

    Article  PubMed  Google Scholar 

  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.2016.6826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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 Elsevier

    Article  CAS  PubMed  Google Scholar 

  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 Group

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Wiley

    Article  CAS  PubMed  Google Scholar 

  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.2011.02.016

    Article  CAS  PubMed  Google Scholar 

  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 Access

    Article  CAS  PubMed  Google Scholar 

  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 Access

    Article  CAS  PubMed  Google Scholar 

  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.2005.7.704

    Article  Google Scholar 

  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/JCI117557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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/s10456-014-9455-0

    Article  CAS  PubMed  Google Scholar 

  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, MD

    Article  CAS  PubMed  Google Scholar 

  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. Wiley

    Article  CAS  PubMed  Google Scholar 

  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.0000000000000062

    Article  Google Scholar 

  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.003186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgment

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

Author information

Authors and Affiliations

  1. Department of Biomedical and Chemical Engineering and Sciences, Florida Institute of Technology, Melbourne, FL, USA

    Kenyatta S. Washington & Chris A. Bashur

Authors
  1. Kenyatta S. Washington
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris A. Bashur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chris A. Bashur .

Editor information

Editors and Affiliations

  1. Department of Orthopaedics School of Medicine, West Virginia University, Morgantown, WV, USA

    Bingyun Li

  2. AO Research Institute Davos, Davos Platz, Graubünden, Switzerland

    Thomas Fintan Moriarty

  3. Department of Chemical Engineering, Northeastern University, Boston, MA, USA

    Thomas Webster

  4. Department of Mechanical Engineering, University of Manitoba, Winnipeg, MB, Canada

    Malcolm Xing

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Washington, K.S., Bashur, C.A. (2020). Gasotransmitters: Antimicrobial Properties and Impact on Cell Growth for Tissue Engineering. In: Li, B., Moriarty, T., Webster, T., Xing, M. (eds) Racing for the Surface. Springer, Cham. https://doi.org/10.1007/978-3-030-34471-9_8

Download citation

Publish with us

Policies and ethics

Search

Navigation