Skip to main content
SpringerLink
Log in

Oxidant-Induced Models of Vascular Leak

  • Chapter
  • First Online:
Measuring Oxidants and Oxidative Stress in Biological Systems

Part of the book series: Biological Magnetic Resonance ((BIMR,volume 34))

  • 576 Accesses

Abstract

The vascular endothelium is an organ that regulates mass transfer between blood and various tissues around the body. Thus, vascular leak, the exchange of fluid between the vasculature and the interstitium of surrounding tissue, is an essential physiological process. The rate of vascular leak is determined by the tightness of the vascular barrier, which is composed of a monolayer of endothelial cells that form the inner lining of blood vessels. This in turn is regulated by redox-dependent modifications to the cytoskeletons of endothelial cells and the cell–cell junctions between them. Thus, understanding redox-dependent regulation of endothelial barrier function is of significant scientific interest. However, the impetus for this area of inquiry extends well beyond scientific curiosity: In several cardiovascular, renal, and metabolic diseases, oxidative stress leads to pathologically enhancement of vascular leak, contributing to thrombogenesis, and other deleterious effects. Thus, understanding the development and consequences of oxidant-induced pathological vascular leak is of paramount importance to the development of effective therapies. A variety of experimental models and measurement techniques are available for the investigation of oxidant-induced vascular leak in preparations ranging from cells to whole organisms. In this chapter, we discuss the mechanisms underlying oxidant modulation of vascular leak, various experimental models of this phenomenon, and methods to assess structure and function of the vascular endothelium. Particular emphasis is placed on selecting the experimental models and measurement techniques that are most appropriate to the research question under investigation.

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. Radeva MY, Waschke J. Mind the gap: mechanisms regulating the endothelial barrier. Acta Physiol (Oxf). 2018;222(1).

    Google Scholar 

  2. Schlingmann B, Molina SA, Koval M. Claudins: gatekeepers of lung epithelial function. Semin Cell Dev Biol. 2015;42:47–57.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Sukriti S, Tauseef M, Yazbeck P, Mehta D. Mechanisms regulating endothelial permeability. Pulm Circ. 2014;4:535–51.

    PubMed  PubMed Central  Google Scholar 

  4. Bravi L, Dejana E, Lampugnani MG. VE-cadherin at a glance. Cell Tissue Res. 2014;355:515–22.

    CAS  PubMed  Google Scholar 

  5. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 2006;86:279–367.

    CAS  PubMed  Google Scholar 

  6. Begandt D, Good ME, Keller AS, DeLalio LJ, Rowley C, Isakson BE, Figueroa XF. Pannexin channel and connexin hemichannel expression in vascular function and inflammation. BMC Cell Biol. 2017;18:2.

    PubMed  PubMed Central  Google Scholar 

  7. Tarbell JM, Cancel LM. The glycocalyx and its significance in human medicine. J Intern Med. 2016;280:97–113.

    CAS  PubMed  Google Scholar 

  8. Alphonsus CS, Rodseth RN. The endothelial glycocalyx: a review of the vascular barrier. Anaesthesia. 2014;69:777–84.

    CAS  PubMed  Google Scholar 

  9. Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol. 2004;557:889–907.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Levick JR. A two-dimensional morphometry-based model of interstitial and transcapillary flow in rabbit synovium. Exp Physiol. 1991;76:905–21.

    CAS  PubMed  Google Scholar 

  11. Jacob M, Bruegger D, Rehm M, Stoeckelhuber M, Welsch U, Conzen P, Becker BF. The endothelial glycocalyx affords compatibility of Starling’s principle and high cardiac interstitial albumin levels. Cardiovasc Res. 2007;73:575–86.

    CAS  PubMed  Google Scholar 

  12. Di A, Mehta D, Malik AB. ROS-activated calcium signaling mechanisms regulating endothelial barrier function. Cell Calcium. 2016;60:163–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Usatyuk PV, Natarajan V. Hydroxyalkenals and oxidized phospholipids modulation of endothelial cytoskeleton, focal adhesion and adherens junction proteins in regulating endothelial barrier function. Microvasc Res. 2012;83:45–55.

    CAS  PubMed  Google Scholar 

  14. Boueiz A, Hassoun PM. Regulation of endothelial barrier function by reactive oxygen and nitrogen species. Microvasc Res. 2009;77:26–34.

    CAS  PubMed  Google Scholar 

  15. Zhang X, Sun D, Song JW, Zullo J, Lipphardt M, Coneh-Gould L, Goligorsky MS. Endothelial cell dysfunction and glycocalyx—a vicious circle. Matrix Biol. 2018;71–72:421–31.

    PubMed  Google Scholar 

  16. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res. 2000;87:840–4.

    CAS  PubMed  Google Scholar 

  17. Petrie JR, Guzik TJ, Touyz RM. Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms. Can J Cardiol. 2018;34:575–84.

    PubMed  PubMed Central  Google Scholar 

  18. Pechlivani N, Ajjan RA. Thrombosis and vascular inflammation in diabetes: mechanisms and potential therapeutic targets. Front Cardiovasc Med. 2018;5:1.

    PubMed  PubMed Central  Google Scholar 

  19. Shi Y, Hu FB. The global implications of diabetes and cancer. Lancet. 2014;383:1947–8.

    PubMed  Google Scholar 

  20. Disease GBD, Injury I, Prevalence C. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1545–602.

    Google Scholar 

  21. Mortality GBD and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1459–544.

    Google Scholar 

  22. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Barker-Collo S, Bartels DH, Bell ML, Benjamin EJ, Bennett D, Bhalla K, Bikbov B, Bin Abdulhak A, Birbeck G, Blyth F, Bolliger I, Boufous S, Bucello C, Burch M, Burney P, Carapetis J, Chen H, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahodwala N, De Leo D, Degenhardt L, Delossantos A, Denenberg J, Des Jarlais DC, Dharmaratne SD, Dorsey ER, Driscoll T, Duber H, Ebel B, Erwin PJ, Espindola P, Ezzati M, Feigin V, Flaxman AD, Forouzanfar MH, Fowkes FG, Franklin R, Fransen M, Freeman MK, Gabriel SE, Gakidou E, Gaspari F, Gillum RF, Gonzalez-Medina D, Halasa YA, Haring D, Harrison JE, Havmoeller R, Hay RJ, Hoen B, Hotez PJ, Hoy D, Jacobsen KH, James SL, Jasrasaria R, Jayaraman S, Johns N, Karthikeyan G, Kassebaum N, Keren A, Khoo JP, Knowlton LM, Kobusingye O, Koranteng A, Krishnamurthi R, Lipnick M, Lipshultz SE, Ohno SL, Mabweijano J, MacIntyre MF, Mallinger L, March L, Marks GB, Marks R, Matsumori A, Matzopoulos R, Mayosi BM, McAnulty JH, McDermott MM, McGrath J, Mensah GA, Merriman TR, Michaud C, Miller M, Miller TR, Mock C, Mocumbi AO, Mokdad AA, Moran A, Mulholland K, Nair MN, Naldi L, Narayan KM, Nasseri K, Norman P, O’Donnell M, Omer SB, Ortblad K, Osborne R, Ozgediz D, Pahari B, Pandian JD, Rivero AP, Padilla RP, Perez-Ruiz F, Perico N, Phillips D, Pierce K, Pope CA III, Porrini E, Pourmalek F, Raju M, Ranganathan D, Rehm JT, Rein DB, Remuzzi G, Rivara FP, Roberts T, De Leon FR, Rosenfeld LC, Rushton L, Sacco RL, Salomon JA, Sampson U, Sanman E, Schwebel DC, Segui-Gomez M, Shepard DS, Singh D, Singleton J, Sliwa K, Smith E, Steer A, Taylor JA, Thomas B, Tleyjeh IM, Towbin JA, Truelsen T, Undurraga EA, Venketasubramanian N, Vijayakumar L, Vos T, Wagner GR, Wang M, Wang W, Watt K, Weinstock MA, Weintraub R, Wilkinson JD, Woolf AD, Wulf S, Yeh PH, Yip P, Zabetian A, Zheng ZJ, Lopez AD, Murray CJ, AlMazroa MA, Memish ZA. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2095–128.

    PubMed  Google Scholar 

  23. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121–35.

    CAS  PubMed  Google Scholar 

  24. Hastie LE, Patton WF, Hechtman HB, Shepro D. Filamin redistribution in an endothelial cell reoxygenation injury model. Free Radic Biol Med. 1997;22:955–66.

    CAS  PubMed  Google Scholar 

  25. Gavard J. Endothelial permeability and VE-cadherin: a wacky comradeship. Cell Adhes Migr. 2014;8:158–64.

    Google Scholar 

  26. Kurzelewski M, Czarnowska E, Beresewicz A. Superoxide- and nitric oxide-derived species mediate endothelial dysfunction, endothelial glycocalyx disruption, and enhanced neutrophil adhesion in the post-ischemic guinea-pig heart. J Physiol Pharmacol. 2005;56:163–78.

    CAS  PubMed  Google Scholar 

  27. Czarnowska E, Karwatowska-Prokopczuk E. Ultrastructural demonstration of endothelial glycocalyx disruption in the reperfused rat heart. Involvement of oxygen free radicals. Basic Res Cardiol. 1995;90:357–64.

    CAS  PubMed  Google Scholar 

  28. Schafer C, Walther S, Schafer M, Dieterich L, Kasseckert S, Abdallah Y, Piper HM. Inhibition of contractile activation reduces reoxygenation-induced endothelial gap formation. Cardiovasc Res. 2003;58:149–55.

    CAS  PubMed  Google Scholar 

  29. Zoni-Berisso M, Lercari F, Carazza T, Domenicucci S. Epidemiology of atrial fibrillation: European perspective. Clin Epidemiol. 2014;6:213–20.

    PubMed  PubMed Central  Google Scholar 

  30. Kim MH, Johnston SS, Chu BC, Dalal MR, Schulman KL. Estimation of total incremental health care costs in patients with atrial fibrillation in the United States. Circ Cardiovasc Qual Outcomes. 2011;4:313–20.

    PubMed  Google Scholar 

  31. Gramley F, Lorenzen J, Jedamzik B, Gatter K, Koellensperger E, Munzel T, Pezzella F. Atrial fibrillation is associated with cardiac hypoxia. Cardiovasc Pathol. 2010;19:102–11.

    PubMed  Google Scholar 

  32. Kimura T, Takatsuki S, Inagawa K, Katsumata Y, Nishiyama T, Nishiyama N, Fukumoto K, Aizawa Y, Tanimoto Y, Tanimoto K, Fukuda K. Serum inflammation markers predicting successful initial catheter ablation for atrial fibrillation. Heart Lung Circ. 2014;23:636–43.

    PubMed  Google Scholar 

  33. Li J, Solus J, Chen Q, Rho YH, Milne G, Stein CM, Darbar D. Role of inflammation and oxidative stress in atrial fibrillation. Heart Rhythm. 2010;7:438–44.

    PubMed  Google Scholar 

  34. Ogi H, Nakano Y, Niida S, Dote K, Hirai Y, Suenari K, Tonouchi Y, Oda N, Makita Y, Ueda S, Kajihara K, Imai K, Sueda T, Chayama K, Kihara Y. Is structural remodeling of fibrillated atria the consequence of tissue hypoxia? Circ J. 2010;74:1815–21.

    CAS  PubMed  Google Scholar 

  35. Scridon A, Morel E, Nonin-Babary E, Girerd N, Fernandez C, Chevalier P. Increased intracardiac vascular endothelial growth factor levels in patients with paroxysmal, but not persistent atrial fibrillation. Europace. 2012;14:948–53.

    PubMed  Google Scholar 

  36. Seko Y, Nishimura H, Takahashi N, Ashida T, Nagai R. Serum levels of vascular endothelial growth factor and transforming growth factor-beta1 in patients with atrial fibrillation undergoing defibrillation therapy. Jpn Heart J. 2000;41:27–32.

    CAS  PubMed  Google Scholar 

  37. Polovina MM, Lip GY, Potpara TS. Endothelial (dys)function in lone atrial fibrillation. Curr Pharm Des. 2015;21:622–45.

    CAS  PubMed  Google Scholar 

  38. Harling L, Lambert J, Ashrafian H, Darzi A, Gooderham NJ, Athanasiou T. Pre-operative serum VCAM-1 as a biomarker of atrial fibrillation after coronary artery bypass grafting. J Cardiothorac Surg. 2017;12:70.

    PubMed  PubMed Central  Google Scholar 

  39. Willeit K, Pechlaner R, Willeit P, Skroblin P, Paulweber B, Schernthaner C, Toell T, Egger G, Weger S, Oberhollenzer M, Kedenko L, Iglseder B, Bonora E, Schett G, Mayr M, Willeit J, Kiechl S. Association between vascular cell adhesion molecule 1 and atrial fibrillation. JAMA Cardiol. 2017;2:516–23.

    PubMed  PubMed Central  Google Scholar 

  40. Verdejo H, Roldan J, Garcia L, Del Campo A, Becerra E, Chiong M, Mellado R, Garcia A, Zalaquett R, Braun S, Garayar B, Gonzalez S, Lavandero S, Corbalan R. Systemic vascular cell adhesion molecule-1 predicts the occurrence of post-operative atrial fibrillation. Int J Cardiol. 2011;150:270–6.

    PubMed  Google Scholar 

  41. McMurray JJ, Pfeffer MA. Heart failure. Lancet. 2005;365:1877–89.

    PubMed  Google Scholar 

  42. Voigt J, Sasha John M, Taylor A, Krucoff M, Reynolds MR, Michael Gibson C. A reevaluation of the costs of heart failure and its implications for allocation of health resources in the United States. Clin Cardiol. 2014;37:312–21.

    PubMed  PubMed Central  Google Scholar 

  43. Gevaert AB, Lemmens K, Vrints CJ, Van Craenenbroeck EM. Targeting endothelial function to treat heart failure with preserved ejection fraction: the promise of exercise training. Oxidative Med Cell Longev. 2017;2017:4865756.

    Google Scholar 

  44. Wray DW, Amann M, Richardson RS. Peripheral vascular function, oxygen delivery and utilization: the impact of oxidative stress in aging and heart failure with reduced ejection fraction. Heart Fail Rev. 2017;22:149–66.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Lewis GA, Schelbert EB, Williams SG, Cunnington C, Ahmed F, McDonagh TA, Miller CA. Biological phenotypes of heart failure with preserved ejection fraction. J Am Coll Cardiol. 2017;70:2186–200.

    PubMed  Google Scholar 

  46. Roe AT, Sjaastad I, Louch WE. Heart failure with preserved ejection fraction. Tidsskr Nor Laegeforen. 2017;137.

    Google Scholar 

  47. Matter K, Balda MS. Functional analysis of tight junctions. Methods. 2003;30:228–34.

    CAS  PubMed  Google Scholar 

  48. Nooteboom A, Hendriks T, Otteholler I, van der Linden CJ. Permeability characteristics of human endothelial monolayers seeded on different extracellular matrix proteins. Mediat Inflamm. 2000;9:235–41.

    CAS  Google Scholar 

  49. Sliman SM, Patel RB, Cruff JP, Kotha SR, Newland CA, Schrader CA, Sherwani SI, Gurney TO, Magalang UJ, Parinandi NL. Adiponectin protects against hyperoxic lung injury and vascular leak. Cell Biochem Biophys. 2013;67:399–414.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. McRae M, LaFratta LM, Nguyen BM, Paris JJ, Hauser KF, Conway DE. Characterization of cell-cell junction changes associated with the formation of a strong endothelial barrier. Tissue Barriers. 2018;6:e1405774.

    PubMed  PubMed Central  Google Scholar 

  51. Szulcek R, Bogaard HJ, van Nieuw Amerongen GP. Electric cell-substrate impedance sensing for the quantification of endothelial proliferation, barrier function, and motility. J Vis Exp. 2014;(85):51300.

    Google Scholar 

  52. Giaever I, Keese CR. Monitoring fibroblast behavior in tissue culture with an applied electric field. Proc Natl Acad Sci U S A. 1984;81:3761–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Sliman SM, Eubank TD, Kotha SR, Kuppusamy ML, Sherwani SI, Butler ES, Kuppusamy P, Roy S, Marsh CB, Stern DM, Parinandi NL. Hyperglycemic oxoaldehyde, glyoxal, causes barrier dysfunction, cytoskeletal alterations, and inhibition of angiogenesis in vascular endothelial cells: aminoguanidine protection. Mol Cell Biochem. 2010;333:9–26.

    CAS  PubMed  Google Scholar 

  54. Duarte D, Hawkins ED, Akinduro O, Ang H, De Filippo K, Kong IY, Haltalli M, Ruivo N, Straszkowski L, Vervoort SJ, McLean C, Weber TS, Khorshed R, Pirillo C, Wei A, Ramasamy SK, Kusumbe AP, Duffy K, Adams RH, Purton LE, Carlin LM, Lo Celso C. Inhibition of endosteal vascular niche remodeling rescues hematopoietic stem cell loss in AML. Cell Stem Cell. 2018;22:64–77.e6.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Gomez-Gelvez JC, Salama ME, Perkins SL, Leavitt M, Inamdar KV. Prognostic impact of tumor microenvironment in diffuse large B-cell lymphoma uniformly treated with R-CHOP chemotherapy. Am J Clin Pathol. 2016;145:514–23.

    PubMed  Google Scholar 

  56. Cai H. Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc Res. 2005;68:26–36.

    CAS  PubMed  Google Scholar 

  57. Rahman NA, Rasil A, Meyding-Lamade U, Craemer EM, Diah S, Tuah AA, Muharram SH. Immortalized endothelial cell lines for in vitro blood-brain barrier models: a systematic review. Brain Res. 1642;2016:532–45.

    Google Scholar 

  58. Bouis D, Hospers GA, Meijer C, Molema G, Mulder NH. Endothelium in vitro: a review of human vascular endothelial cell lines for blood vessel-related research. Angiogenesis. 2001;4:91–102.

    CAS  PubMed  Google Scholar 

  59. Haorah J, Knipe B, Leibhart J, Ghorpade A, Persidsky Y. Alcohol-induced oxidative stress in brain endothelial cells causes blood-brain barrier dysfunction. J Leukoc Biol. 2005;78:1223–32.

    CAS  PubMed  Google Scholar 

  60. Schreibelt G, Kooij G, Reijerkerk A, van Doorn R, Gringhuis SI, van der Pol S, Weksler BB, Romero IA, Couraud PO, Piontek J, Blasig IE, Dijkstra CD, Ronken E, de Vries HE. Reactive oxygen species alter brain endothelial tight junction dynamics via RhoA, PI3 kinase, and PKB signaling. FASEB J. 2007;21:3666–76.

    CAS  PubMed  Google Scholar 

  61. Usatyuk PV, Romer LH, He D, Parinandi NL, Kleinberg ME, Zhan S, Jacobson JR, Dudek SM, Pendyala S, Garcia JG, Natarajan V. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J Biol Chem. 2007;282:23284–95.

    CAS  PubMed  Google Scholar 

  62. Usatyuk PV, Vepa S, Watkins T, He D, Parinandi NL, Natarajan V. Redox regulation of reactive oxygen species-induced p38 MAP kinase activation and barrier dysfunction in lung microvascular endothelial cells. Antioxid Redox Signal. 2003;5:723–30.

    CAS  PubMed  Google Scholar 

  63. Shi S, Garcia JG, Roy S, Parinandi NL, Natarajan V. Involvement of c-Src in diperoxovanadate-induced endothelial cell barrier dysfunction. Am J Physiol Lung Cell Mol Physiol. 2000;279:L441–51.

    CAS  PubMed  Google Scholar 

  64. Patel RB, Kotha SR, Sauers LA, Malireddy S, Gurney TO, Gupta NN, Elton TS, Magalang UJ, Marsh CB, Haley BE, Parinandi NL. Thiol-redox antioxidants protect against lung vascular endothelial cytoskeletal alterations caused by pulmonary fibrosis inducer, bleomycin: comparison between classical thiol-protectant, N-acetyl-L-cysteine, and novel thiol antioxidant, N,N′-bis-2-mercaptoethyl isophthalamide. Toxicol Mech Methods. 2012;22:383–96.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Parinandi NL, Sharma A, Eubank TD, Kaufman BF, Kutala VK, Marsh CB, Ignarro LJ, Kuppusamy P. Nitroaspirin (NCX-4016), an NO donor, is antiangiogenic through induction of loss of redox-dependent viability and cytoskeletal reorganization in endothelial cells. Antioxid Redox Signal. 2007;9:1837–49.

    CAS  PubMed  Google Scholar 

  66. Kenakin T. Isolated blood vessel assays. Curr Protoc Pharmacol. 2001;Chapter 4:Unit4 4.

    Google Scholar 

  67. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JA, Kajiya F. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol. 2003;285:H722–6.

    CAS  PubMed  Google Scholar 

  68. Shreim SG, Steward E, Botvinick EL. Extending vaterite microviscometry to ex vivo blood vessels by serial calibration. Biomed Opt Express. 2012;3:37–47.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, The Ohio State University, Columbus, OH, USA

    Rengasayee Veeraraghavan & Thomas J. Hund

  2. Bob and Corinne Frick Center for Heart Failure and Arrhythmia, The Ohio State University Wexner Medical Center, Columbus, OH, USA

    Rengasayee Veeraraghavan, Narasimham L. Parinandi & Thomas J. Hund

  3. Dorothy M. Davis Heart and Lung Research Institute, College of Medicine, The Ohio State University Wexner Medical Center, Columbus, OH, USA

    Rengasayee Veeraraghavan, Narasimham L. Parinandi & Thomas J. Hund

  4. Department of Physiology and Cell Biology, College of Medicine, The Ohio State University, Columbus, OH, USA

    Rengasayee Veeraraghavan

Authors
  1. Rengasayee Veeraraghavan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Narasimham L. Parinandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas J. Hund
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rengasayee Veeraraghavan .

Editor information

Editors and Affiliations

  1. Department of Chemistry and Biochemistry, University of Denver, Centennial, CO, USA

    Lawrence J. Berliner

  2. Department of Internal Medicine, Division of Pulmonary, Critical Care, and Sleep Medicine, Ohio State University College of Medicine, Dorothy M. Davis Heart and Lung Research Institute, Columbus, OH, USA

    Narasimham L. Parinandi

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

Veeraraghavan, R., Parinandi, N.L., Hund, T.J. (2020). Oxidant-Induced Models of Vascular Leak. In: Berliner, L., Parinandi, N. (eds) Measuring Oxidants and Oxidative Stress in Biological Systems. Biological Magnetic Resonance, vol 34. Springer, Cham. https://doi.org/10.1007/978-3-030-47318-1_6

Download citation

Publish with us

Policies and ethics

Search

Navigation