Abstract

Review Article

A mouse model of coronary microvacsular disease using a photochemical approach

Xinlu Wang, Fang Liu and Zhen W. Zhuang*

Published: 18 September, 2019 | Volume 4 - Issue 3 | Pages: 120-130

The development of reproducible rodent models of coronary microvascular disease (MVD) is essential for the early detection, treatment, and mechanism study of the pathophysiology. We hypothesized that endothelial dysfunction and subsequent microthrombi in the coronary arterioles, two early events in clinical coronary MVD, could be reproduced by photochemical reaction (PCR) technology in mice hearts. After rose bengal (one of photosensitizers) was administrated systemically, a green light was locally used to activate the photosensitizer, inducing over-production of oxidative stress in the heart. Following PCR, animals demonstrated reproducible endothelial injury, occlusion in arterioles, focal ischemia, and infarct-let with preserved cardiac function. Our technique has proven to be a reliable and reproducible means of creating coronary MVD in mice. We believe that this is an ideal model for developing a novel molecular tracer for earlier detection of coronary MVD, for testing new anti-fibrinolytic drugs, and for investigating the complex pathophysiology of coronary MVD. The protocol for establishing this model takes about thirty to forty minutes.

Read Full Article HTML DOI: 10.29328/journal.jccm.1001052 Cite this Article Read Full Article PDF

References

  1. Shaw LJ, Merz CN, Pepine CJ, Reis SE, Bittner V, et al. Women's Ischemia Syndrome Evaluation (WISE) Investigators. The economic burden of angina in women with suspected ischemic heart disease: results from the National Institutes of Health--National Heart, Lung, and Blood Institute--sponsored Women's Ischemia Syndrome Evaluation. Circulation. 2006; 114: 894-904. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16923752
  2. Reis SE, Holubkov R, Conrad Smith AJ, Kelsey SF, Sharaf BL, et al. WISE Investigators. Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study. Am Heart J. 2001; 141: 735-741. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11320360
  3. Pepine CJ, Anderson RD, Sharaf BL, Reis SE, Smith KM, et al. Coronary microvascular reactivity to adenosine predicts adverse outcome in women evaluated for suspected ischemia results from the National Heart, Lung and Blood Institute WISE (Women's Ischemia Syndrome Evaluation) study. J Am Coll Cardiol. 2010; 55: 2825-2832. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20579539
  4. Likoff W, Segal BL, Kasparian H. Paradox of normal selective coronary arteriograms in patients considered to have unmistakable coronary heart disease. N Engl J Med. 1967; 276: 1063-1066. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/6025663
  5. Mosseri M, Yarom R, Gotsman M, Hasin Y. Histologic evidence for small-vessel coronary artery disease in patients with angina pectoris and patent large coronary arteries. Circulation. 1986; 74: 964-972. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/3769180
  6. Suzuki H, Takeyama Y, Koba S, Suwa Y, Katagiri T. Small vessel pathology and coronary hemodynamics in patients with microvascular angina. Int J Cardiol. 1994; 43: 139-150. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/8181868
  7. Zhuang ZW, Huang Y, Ju R, Maxfield MW, Ren Y, et al. Molecular imaging of factor XIII activity for the early detection of mouse coronary microvascular disease. Theranostics. 2019; 9: 1474-1489. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30867844
  8. Granger D, Rodrigues S, Yildirim A, Senchenkova E. Microvascular responses to cardiovascular risk factors. Microcirculation. 2010; 17: 192-205. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20374483
  9. Shaw LJ, Bairey Merz CN, Pepine CJ, Reis SE, Bittner V, et al. Insights from the NHLBI- Sponsored Women's Ischemia Syndrome Evaluation (WISE) Study: Part I: gender differences in traditional and novel risk factors, symptom evaluation, and gender-optimized diagnostic strategies. J Am Coll Cardiol. 2006; 47(3 Suppl): S4-S20. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16458170
  10. Pepine CJ, Kerensky RA, Lambert CR, Smith KM, von Mering GO, et al. Some thoughts on the vasculopathy of women with ischemic heart disease. J Am Coll Cardiol. 2006; 47(3 Suppl): S30-35. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16458168
  11. Kaski JC, Aldama G, Cosín-Sales J. Cardiac syndrome X. Diagnosis, pathogenesis and management. Am J Cardiovasc Drugs. 2004; 4: 179-194. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15134470
  12. Versari D, Daghini E, Virdis A, Ghiadoni L, Taddei S. Endothelial Dysfunction as a Target for Prevention of Cardiovascular Disease. Diabetes Care. 2009; 32: S314-S321. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19875572
  13. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular disease: the role of oxidant stress. Circ Res. 2000; 87: 840-844. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11073878
  14. Egashira K, Hirooka Y, Kuga T, Mohri M, Takeshita A. Effects of L-arginine supplementation on endothelium-dependent coronary vasodilatation in patients with angina pectoris and normal coronary arteriograms. Circulation. 1996; 94: 130-134. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/8674170
  15. Tousoulis D, Briasoulis A, Papageorgiou N, Tsioufis C, Tsiamis E, et al. Oxidative Stress and Endothelial Function: Therapeutic Interventions. Recent Pat Cardiovasc Drug Discov. 2011; 6: 103-114. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21513492
  16. Pennathur S, Heinecke JW. Oxidative stress and endothelial dysfunction in vascular disease. Curr Diab Rep. 2007; 7: 257-264. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17686400
  17. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res. 2000; 86: 494-501. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10720409
  18. Madamanchi NR, Runge MS. Mitochondrial dysfunction in atherosclerosis. Circ Res. 2007; 100: 460-473. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17332437
  19. Caccese D, Pratico D, Ghiselli A, Natoli S, Pignatelli P, et al. Superoxide anion and hydroxyl radical release by collagen-induced platelet aggregation: role of arachidonic acid metabolism. Thromb Haemost. 2000; 83: 485-490. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/10744158
  20. Maki J, Hirano M, Hoka S, Kanaide H, Hirano K. Involvement of reactive oxygen species in thrombin-induced pulmonary vasoconstriction. Am J Respir Crit Care Med. 2010; 182: 1435-1444. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20639439
  21. Zhuang ZW, Shi J, Rhodes JM, Tsapakos MJ, Simons M. Challenging the surgical rodent hindlimb ischemia model with the miniinterventional technique. J Vasc Interv Radiol. 2011; 22: 1437-1446. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21459613
  22. Nichols TC, Bellinger DA, Reddick RL, Read MS, Koch GG, et al. Role of von Willebrand factor in arterial thrombosis: studies in normal and von Willebrand disease pigs. Circulation. 1991; 83: IV56-IV64. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/2040072
  23. Malyar NM, Lerman LO, Gössl M, Beighley PE, Ritman EL. Relationship between Surface Area of Nonperfused Myocardium and Extravascular Extraction of Contrast Agent following Coronary Microembolization. Am J Physiol Regul Integr Comp Physiol. 2011; 301: R430-R437. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21543631
  24. Li L, Li DH, Qu N, Wen WM, Huang WQ. The role of ERK1/2 signaling pathway in coronary microembolization-induced rat myocardial inflammation and injury. Cardiology. 2010; 117: 207-215. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21150201
  25. Carlsson M, Wilson M, Martin AJ, Saeed M. Myocardial microinfarction after coronary microembolization in swine: MR imaging characterization. Radiology. 2009; 250: 703-713. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19164123
  26. Falk E. Unstable angina with fatal outcome: dynamic coronary thrombosis leading to infarction and/or sudden death: autopsy evidence of recurrent mural thrombosis with peripheral embolization culminating in total vascular occlusion. Circulation. 1985; 71: 699-708. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/3971539
  27. Li SM, Zeng K, Wang WW, Zhang FL, Sun XD, et al. Time course of myocardial NF-kappaB activation post coronary microembolization. Zhonghua Xin Xue Guan Bing Za Zhi. 2008; 36: 1016-1020. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19102917
  28. Haft JI, Kranz PD, Albert FJ, Fani K. Intravascular platelet aggregation in the heart induced by norepinephrine. Circulation. 1972; 46: 698-708. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/5072771
  29. Ciulla MM, Paliotti R, Ferrero S, Braidotti P, Esposito A, et al. Left ventricular remodeling after experimental myocardial cryoinjury in rats. J Surg Res. 2004; 116: 91-97. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/14732353
  30. van Amerongen MJ, Harmsen MC, Petersen AH, Popa ER, van Luyn MJ. Cryoinjury: a model of myocardial regeneration. Cardiovascular Pathology. 2008; 17: 23-31. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18160057
  31. Dolmans D, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer. 2003; 3: 380-387. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12724736
  32. Detombe SA, Dunmore-Buyze J, Drangova M. Evaluation of eXIA 160 cardiac-related enhancement in C57BL/6 and BALB/c mice using micro-CT. Contrast Media Mol Imaging. 2012; 7: 240-246. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22434637
  33. Morin RL, Gerber TC, McCollough CH. Radiation dose in computed tomography of the heart. Circulation. 2013; 107: 917-922. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/12591765
  34. Hofmann JJ, Briot A, Enciso J, Zovein AC, Ren S, et al. Endothelial deletion of murine Jag1 leads to valve calcification and congenital heart defects associated with Alagille syndrome. Development. 2012; 139: 4449-4460. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23095891
  35. Landskroner-Eiger S, Qiu C, Perrotta P, Siragusa M, Lee MY, et al. Endothelial miR-17∼92 cluster negatively regulates arteriogenesis via miRNA-19 repression of WNT signaling. Proc Natl Acad Sci USA. 2015; 112: 12812-12817. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26417068Kivelä R, Bry M, Robciuc MR, Räsänen M, Taavitsainen M, et al. VEGF-B-induced vascular growth leads to metabolic reprogramming and ischemia resistance in the heart. EMBO Mol Med. 2014; 6: 307-321. PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24448490

Figures:

Similar Articles

Recently Viewed

Read More

Most Viewed

Read More

Help ?