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Pentagalloyl Glucose and Its Functional Role in Vascular Health: Biomechanics and Drug-Delivery Characteristics

  • Sourav S. Patnaik
  • Dan T. Simionescu
  • Craig J. Goergen
  • Kenneth Hoyt
  • Shashank Sirsi
  • Ender A. Finol
Article
  • 38 Downloads

Abstract

Pentagalloyl glucose (PGG) is an elastin-stabilizing polyphenolic compound that has significant biomedical benefits, such as being a free radical sink, an anti-inflammatory agent, anti-diabetic agent, enzymatic resistant properties, etc. This review article focuses on the important benefits of PGG on vascular health, including its role in tissue mechanics, the different modes of pharmacological administration (e.g., oral, intravenous and endovascular route, intraperitoneal route, subcutaneous route, and nanoparticle based delivery and microbubble-based delivery), and its potential therapeutic role in vascular diseases such as abdominal aortic aneurysms (AAA). In particular, the use of PGG for AAA suppression and prevention has been demonstrated to be effective only in the calcium chloride rat AAA model. Therefore, in this critical review we address the challenges that lie ahead for the clinical translation of PGG as an AAA growth suppressor.

Keywords

Pentagalloyl glucose Abdominal aortic aneurysms Elastin Collagen Drug delivery 

Abbreviations

60Co-γ rays

Cobalt-60 gamma rays

6-Keto-PGF1α

6-Keto-prostaglandin 1α

ADP

Adenosine-5′-diphosphate

ALT

Alanine aminotransferase

AP-1

Activator protein-1

ArA

Arachidonic acid

B16F10

Metastatic mouse melanoma cells

BHK-21 cells

Baby hamster kidney cell

BV-2

Transfected microglial cell line

CAT

Catalase

CC50

50% cytotoxic concentration

Cmax

Maximum serum concentration that a drug achieves in a test area of the body after the drug has been administrated and before the administration of a second dose

CML cell line K56

Human chronic myelogenous leukemia

DMSO

Dimethylsulfoxide

DPPH

2,2-diphenyl-1-picrylhydrazyl

EC 2.3.1.67

Acetyl-CoA:1-alkyl-sn-glycero-3-phosphocholine acetyltransferase

EC50

The concentration of a compound where 50% of its maximal effect is observed

EGF

Epidermal growth factor

FcɛRI

High-affinity IgE receptors

GPIIb/IIIa

Glycoprotein IIb/IIIa inhibitors

GSH-Px

Glutathione peroxidase

HBZY-1 cells

Glomerular mesangial cell line

HPBMC

Human peripheral blood mononuclear cells

HUVECs

Human umbilical vein endothelial cells

IB5

Basic salivary protein

IC50

Half maximal inhibitory concentration

ICAM-1

Intercellular adhesion molecule 1

IL-1

Interleukin-1

IL-4

Interleukin-4

IL-6

Interleukin-6

IL-8

Interleukin-8

IL-10

Interleukin-10

Kd

Dissociation constant—represents ligand-receptor affinity

mBMMCs

Mouse bone marrow-derived mast cells

MCP-1

Monocyte chemoattractant protein 1

NF-kB

Nuclear factor-kB

NO-cGMP pathway

Nitric oxide/cyclic guanosine monophosphate signaling pathway

NOS

Nitric oxide synthase

NR

Not reported

NS3

Nonstructural protein 3

PAF

1-Alkyl-2-acetyl-sn-glycero-3-phosphocholine

PC-3

Human prostate cancer cell line

PMN

Polymorphonuclear leukocyte system

rhALR2

Recombinant human aldose reductase

ROS

Reactive oxygen species

SCID

Severe combined immunodeficiency

SK-MEL-28

Human skin melanoma cell line

SOD

Superoxide dismutase

SP-1

Specificity protein 1

TGF-β1

Transforming growth factor beta 1

Tmax

Time at which the Cmax is observed

TNF-α

Tumor necrosis factor alpha

TXB2

Thromboxane B2

U937

(Pro-) monocytic cell lines

V79-4 cells

Chinese hamster lung fibroblasts

XOD

Xanthine oxidase

Notes

Acknowledgments

The authors have no conflicts of interest to disclose and would like to acknowledge research funding from American Heart Association Award #16CSA28480006. The content is solely the responsibility of the authors and does not necessarily represent the official views of the American Heart Association.

Supplementary material

10439_2018_2145_MOESM1_ESM.docx (96 kb)
Supplementary material 1 (DOCX 95 kb)

References

  1. 1.
    Abdel-Mageed, W. M., S. A. Bayoumi, C. Chen, C. J. Vavricka, L. Li, A. Malik, H. Dai, F. Song, L. Wang, J. Zhang, G. F. Gao, Y. Lv, L. Liu, X. Liu, H. M. Sayed, and L. Zhang. Benzophenone C-glucosides and gallotannins from mango tree stem bark with broad-spectrum anti-viral activity. Bioorgan. Med. Chem. 22:2236–2243, 2014.CrossRefGoogle Scholar
  2. 2.
    Abdelwahed, A., I. Bouhlel, I. Skandrani, K. Valenti, M. Kadri, P. Guiraud, R. Steiman, A. M. Mariotte, K. Ghedira, F. Laporte, M. G. Dijoux-Franca, and L. Chekir-Ghedira. Study of antimutagenic and antioxidant activities of gallic acid and 1,2,3,4,6-pentagalloylglucose from Pistacia lentiscus. Confirmation by microarray expression profiling. Chem. Biol. Interact. 165:1–13, 2007.PubMedCrossRefGoogle Scholar
  3. 3.
    Abdul-Hussien, H., R. Hanemaaijer, J. H. Verheijen, J. H. van Bockel, R. H. Geelkerken, and J. H. Lindeman. Doxycycline therapy for abdominal aneurysm: improved proteolytic balance through reduced neutrophil content. J. Vasc. Surg. 49:741–749, 2009.PubMedCrossRefGoogle Scholar
  4. 4.
    Adolph, R., D. A. Vorp, D. L. Steed, M. W. Webster, M. V. Kameneva, and S. C. Watkins. Cellular content and permeability of intraluminal thrombus in abdominal aortic aneurysm. J. Vasc. Surg. 25:916–926, 1997.PubMedCrossRefGoogle Scholar
  5. 5.
    Allaire, E. Cyclosporine A in patients with small diameter abdominal aortic aneurysm. https://clinicaltrials.gov/show/NCT02225756, 2010.
  6. 6.
    Alkilani, A. Z., M. T. McCrudden, and R. F. Donnelly. Transdermal drug delivery: innovative pharmaceutical developments based on disruption of the barrier properties of the stratum corneum. Pharmaceutics 7:438–470, 2015.PubMedCrossRefGoogle Scholar
  7. 7.
    Appis, A. W., M. J. Tracy, and S. B. Feinstein. Update on the safety and efficacy of commercial ultrasound contrast agents in cardiac applications. Echo Res. Pract. 2:R55–R62, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Bahadar, H., F. Maqbool, K. Niaz, and M. Abdollahi. Toxicity of nanoparticles and an overview of current experimental models. Iran Biomed. J. 20:1–11, 2016.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Bajaj, G., and Y. Yeo. Drug delivery systems for intraperitoneal therapy. Pharm. Res. 27:735–738, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Barenholz, Y. Doxil(R)–the first FDA-approved nano-drug: lessons learned. J. Control Release 160:117–134, 2012.PubMedCrossRefGoogle Scholar
  11. 11.
    Baxter, B. T., Curci, J., Matsumura, J., and Terrin, M. L. Non-invasive treatment of abdominal aortic aneurysm clinical trial. https://clinicaltrials.gov/show/NCT01756833, 2016.
  12. 12.
    Baxter, B. T., V. A. Davis, D. J. Minion, Y. P. Wang, T. G. Lynch, and B. M. McManus. Abdominal aortic aneurysms are associated with altered matrix proteins of the nonaneurysmal aortic segments. J. Vasc. Surg. 19:797–802, 1994; ((Discussion 803)).PubMedCrossRefGoogle Scholar
  13. 13.
    Baxter, N. J., T. H. Lilley, E. Haslam, and M. P. Williamson. Multiple interactions between polyphenols and a salivary proline-rich protein repeat result in complexation and precipitation. Biochemistry 36:5566–5577, 1997.PubMedCrossRefGoogle Scholar
  14. 14.
    Behrendt, P., P. Perin, N. Menzel, D. Banda, S. Pfaender, M. P. Alves, V. Thiel, P. Meuleman, C. C. Colpitts, L. M. Schang, F. W. R. Vondran, Anggakusuma, M. P. Manns, E. Steinmann, and T. Pietschmann. Pentagalloylglucose, a highly bioavailable polyphenolic compound present in Cortex moutan, efficiently blocks hepatitis C virus entry. Antivir. Res. 147:19–28, 2017.PubMedCrossRefGoogle Scholar
  15. 15.
    Bennick, A. Interaction of plant polyphenols with salivary proteins. Crit. Rev. Oral Biol. Med. 13:184–196, 2002.PubMedCrossRefGoogle Scholar
  16. 16.
    Bhimani, R. S., W. Troll, D. Grunberger, and K. Frenkel. Inhibition of oxidative stress in HeLa cells by chemopreventive agents. Cancer Res. 53:4528–4533, 1993.PubMedGoogle Scholar
  17. 17.
    Bicknell, C. D., G. Kiru, E. Falaschetti, J. T. Powell, N. R. Poulter, and A. Collaborators. An evaluation of the effect of an angiotensin-converting enzyme inhibitor on the growth rate of small abdominal aortic aneurysms: a randomized placebo-controlled trial (AARDVARK). Eur. Heart J. 37:3213–3221, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Bing, S. J., M. J. Kim, E. Park, G. Ahn, D. S. Kim, R. K. Ko, N. H. Lee, T. Shin, J. W. Park, and Y. Jee. 1,2,3,4,6-penta-O-galloyl-beta-d-glucose protects splenocytes against radiation-induced apoptosis in murine splenocytes. Biol. Pharm. Bull. 33:1122–1127, 2010.PubMedCrossRefGoogle Scholar
  19. 19.
    Blanchard, J. F., H. K. Armenian, and P. P. Friesen. Risk factors for abdominal aortic aneurysm: results of a case-control study. Am. J. Epidemiol. 151:575–583, 2000.PubMedCrossRefGoogle Scholar
  20. 20.
    Bors, W., L. Y. Foo, N. Hertkorn, C. Michel, and K. Stettmaier. Chemical studies of proanthocyanidins and hydrolyzable tannins. Antioxid. Redox Signal. 3:995–1008, 2001.PubMedCrossRefGoogle Scholar
  21. 21.
    Cai, K., and A. Bennick. Effect of salivary proteins on the transport of tannin and quercetin across intestinal epithelial cells in culture. Biochem. Pharmacol. 72:974–980, 2006.PubMedCrossRefGoogle Scholar
  22. 22.
    Cai, K., A. E. Hagerman, R. E. Minto, and A. Bennick. Decreased polyphenol transport across cultured intestinal cells by a salivary proline-rich protein. Biochem. Pharmacol. 71:1570–1580, 2006.PubMedCrossRefGoogle Scholar
  23. 23.
    Cao, Y., K. B. Himmeldirk, Y. Qian, Y. Ren, A. Malki, and X. Chen. Biological and biomedical functions of penta-O-galloyl-d-glucose and its derivatives. J. Nat. Med. 68:465–472, 2014.PubMedCrossRefGoogle Scholar
  24. 24.
    Carmo, M., L. Colombo, A. Bruno, F. R. M. Corsi, L. Roncoroni, M. S. Cuttin, F. Radice, E. Mussini, and P. G. Settembrini. Alteration of elastin, collagen and their cross-links in abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 23:543–549, 2002.PubMedCrossRefGoogle Scholar
  25. 25.
    Chai, Y., H. J. Lee, A. A. Shaik, K. Nkhata, C. Xing, J. Zhang, S. J. Jeong, S. H. Kim, and J. Lu. Penta-O-galloyl-beta-d-glucose induces G1 arrest and DNA replicative S-phase arrest independently of cyclin-dependent kinase inhibitor 1A, cyclin-dependent kinase inhibitor 1B and P53 in human breast cancer cells and is orally active against triple negative xenograft growth. Breast Cancer Res. 12:R67, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Charlton, A. J., N. J. Baxter, M. L. Khan, A. J. Moir, E. Haslam, A. P. Davies, and M. P. Williamson. Polyphenol/peptide binding and precipitation. J. Agric. Food Chem. 50:1593–1601, 2002.PubMedCrossRefGoogle Scholar
  27. 27.
    Charlton, A. J., N. J. Baxter, T. H. Lilley, E. Haslam, C. J. McDonald, and M. P. Williamson. Tannin interactions with a full-length human salivary proline-rich protein display a stronger affinity than with single proline-rich repeats. FEBS Lett. 382:289–292, 1996.PubMedCrossRefGoogle Scholar
  28. 28.
    Chauhan, S. S., C. A. Gutierrez, M. Thirugnanasambandam, V. De Oliveira, S. C. Muluk, M. K. Eskandari, and E. A. Finol. The association between geometry and wall stress in emergently repaired abdominal aortic aneurysms. Ann. Biomed. Eng. 45:1908–1916, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Chen, Y., and A. E. Hagerman. Characterization of soluble non-covalent complexes between bovine serum albumin and beta-1,2,3,4,6-penta-O-galloyl-d-glucopyranose by MALDI-TOF MS. J. Agric. Food Chem. 52:4008–4011, 2004.PubMedCrossRefGoogle Scholar
  30. 30.
    Chen, Y., and A. E. Hagerman. Reaction pH and protein affect the oxidation products of beta-pentagalloyl glucose. Free Rad. Res. 39:117–124, 2005.CrossRefGoogle Scholar
  31. 31.
    Cheng, J.-T., and Hsu, F.-L. Tannin derivatives and their use for treatment of hypertension. https://www.google.com/patents/US5266319. Google Patents, 1993.
  32. 32.
    Chow, J. P., D. T. Simionescu, A. L. Carter, and A. Simionescu. Immunomodulatory effects of adipose tissue-derived stem cells on elastin scaffold remodeling in diabetes. Tissue Eng. Regen. Med. 13:701–712, 2016.CrossRefGoogle Scholar
  33. 33.
    Chow, J. P., D. T. Simionescu, H. Warner, B. Wang, S. S. Patnaik, J. Liao, and A. Simionescu. Mitigation of diabetes-related complications in implanted collagen and elastin scaffolds using matrix-binding polyphenol. Biomaterials 34:685–695, 2013.PubMedCrossRefGoogle Scholar
  34. 34.
    Chu, A. Healthy Harvest, Hale Heart. J. Cardiovasc. Disord. 1:3, 2014. http://austinpublishinggroup.com/cardiovascular-disorders/fulltext/jcd-v1-id1004.pdf.
  35. 35.
    Chuang, T. H., C. Stabler, A. Simionescu, and D. T. Simionescu. Polyphenol-stabilized tubular elastin scaffolds for tissue engineered vascular grafts. Tissue Eng. A 15:2837–2851, 2009.CrossRefGoogle Scholar
  36. 36.
    Cryan, L. M., L. Bazinet, K. A. Habeshian, S. Cao, J. Clardy, K. A. Christensen, and M. S. Rogers. 1,2,3,4,6-Penta-O-galloyl-beta-d-glucopyranose inhibits angiogenesis via inhibition of capillary morphogenesis gene 2. J. Med. Chem. 56:1940–1945, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Daugherty, A., M. W. Manning, and L. A. Cassis. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J. Clin. Invest. 105:1605–1612, 2000.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    De Jong, W. H., and P. J. Borm. Drug delivery and nanoparticles:applications and hazards. Int. J. Nanomed. 3:133–149, 2008.CrossRefGoogle Scholar
  39. 39.
    Deborde, C., D. T. Simionescu, C. Wright, J. Liao, L. N. Sierad, and A. Simionescu. Stabilized collagen and elastin-based scaffolds for mitral valve tissue engineering. Tissue Eng. A 22:1241–1251, 2016.CrossRefGoogle Scholar
  40. 40.
    Dimcevski, G., S. Kotopoulis, T. Bjanes, D. Hoem, J. Schjott, B. T. Gjertsen, M. Biermann, A. Molven, H. Sorbye, E. McCormack, M. Postema, and O. H. Gilja. A human clinical trial using ultrasound and microbubbles to enhance gemcitabine treatment of inoperable pancreatic cancer. J. Control Release 243:172–181, 2016.PubMedCrossRefGoogle Scholar
  41. 41.
    Dobreva, M. A., R. A. Frazier, I. Mueller-Harvey, L. A. Clifton, A. Gea, and R. J. Green. Binding of pentagalloyl glucose to two globular proteins occurs via multiple surface sites. Biomacromolecules 12:710–715, 2011.PubMedCrossRefGoogle Scholar
  42. 42.
    Dong, H., S. X. Chen, R. M. Kini, and H. X. Xu. Effects of tannins from Geum japonicum on the catalytic activity of thrombin and factor Xa of blood coagulation cascade. J. Nat. Prod. 61:1356–1360, 1998.PubMedCrossRefGoogle Scholar
  43. 43.
    Emeto, T. I., F. O. Alele, A. M. Smith, F. M. Smith, T. Dougan, and J. Golledge. Use of nanoparticles as contrast agents for the functional and molecular imaging of abdominal aortic aneurysm. Front. Cardiovasc. Med. 4:16, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Fajemiroye, J. O., K. Adam, K. Z. Jordan, C. E. Alves, and A. A. Aderoju. Evaluation of anxiolytic and antidepressant-like activity of aqueous leaf extract of Nymphaea Lotus Linn. in Mice. Iran J. Pharm. Res. 17:613–626, 2018.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Feinstein, S. B., J. Cheirif, F. J. Ten Cate, P. R. Silverman, P. A. Heidenreich, C. Dick, R. M. Desir, W. F. Armstrong, M. A. Quinones, and P. M. Shah. Safety and efficacy of a new transpulmonary ultrasound contrast agent: initial multicenter clinical results. J. Am. Coll. Cardiol. 16:316–324, 1990.PubMedCrossRefGoogle Scholar
  46. 46.
    Feldman, K. S., K. Sahasrabudhe, M. D. Lawlor, S. L. Wilson, C. H. Lang, and W. J. Scheuchenzuber. In vitro and In vivo inhibition of LPS-stimulated tumor necrosis factor-alpha secretion by the gallotannin beta-d-pentagalloylglucose. Bioorgan. Med. Chem. Lett. 11:1813–1815, 2001.CrossRefGoogle Scholar
  47. 47.
    Fercana, G., D. Bowser, M. Portilla, E. M. Langan, C. G. Carsten, D. L. Cull, L. N. Sierad, and D. T. Simionescu. Platform technologies for decellularization, tunic-specific cell seeding, and in vitro conditioning of extended length, small diameter vascular grafts. Tissue Eng. C 20:1016–1027, 2014.CrossRefGoogle Scholar
  48. 48.
    Ferguson, C. D., P. Clancy, B. Bourke, P. J. Walker, A. Dear, T. Buckenham, P. Norman, and J. Golledge. Association of statin prescription with small abdominal aortic aneurysm progression. Am. Heart J. 159:307–313, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Geers, B., I. Lentacker, N. N. Sanders, J. Demeester, S. Meairs, and S. C. De Smedt. Self-assembled liposome-loaded microbubbles: the missing link for safe and efficient ultrasound triggered drug-delivery. J. Control Release 152:249–256, 2011.PubMedCrossRefGoogle Scholar
  50. 50.
    Genfa, L., Z. Jiang, Z. Hong, Z. Yimin, W. Liangxi, W. Guo, H. Ming, J. Donglen, and W. Lizhao. The screening and isolation of an effective anti-endotoxin monomer from Radix Paeoniae Rubra using affinity biosensor technology. Int. Immunopharmacol. 5:1007–1017, 2005.PubMedCrossRefGoogle Scholar
  51. 51.
    Gilabert, R., L. Bunesch, M. I. Real, A. Garcia-Criado, M. Burrel, J. R. Ayuso, M. Barrufet, X. Montana, and V. Riambau. Evaluation of abdominal aortic aneurysm after endovascular repair: prospective validation of contrast-enhanced US with a second-generation US contrast agent. Radiology 264:269–277, 2012.PubMedCrossRefGoogle Scholar
  52. 52.
    Golledge, J., and P. E. Norman. Current status of medical management for abdominal aortic aneurysm. Atherosclerosis 217:57–63, 2011.PubMedCrossRefGoogle Scholar
  53. 53.
    Golledge, J., P. E. Norman, M. P. Murphy, and R. L. Dalman. Challenges and opportunities in limiting abdominal aortic aneurysm growth. J. Vasc. Surg. 65:225–233, 2017.PubMedCrossRefGoogle Scholar
  54. 54.
    Golledge, J., and J. T. Powell. Medical management of abdominal aortic aneurysm. Eur. J. Vasc. Endovasc. Surg. 34:267–273, 2007.PubMedCrossRefGoogle Scholar
  55. 55.
    Goto, H., Y. Shimada, Y. Akechi, K. Kohta, M. Hattori, and K. Terasawa. Endothelium-dependent vasodilator effect of extract prepared from the roots of Paeonia lactiflora on isolated rat aorta. Planta Med. 62:436–439, 1996.PubMedCrossRefGoogle Scholar
  56. 56.
    Gramiak, R., and P. M. Shah. Echocardiography of the aortic root. Invest. Radiol. 3:356–366, 1968.PubMedCrossRefGoogle Scholar
  57. 57.
    Guessous, I., D. Periard, D. Lorenzetti, J. Cornuz, and W. A. Ghali. The efficacy of pharmacotherapy for decreasing the expansion rate of abdominal aortic aneurysms: a systematic review and meta-analysis. PLoS ONE 3:e1895, 2008.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Gupta, A., D. Thompson, A. Whitehouse, T. Collier, B. Dahlof, N. Poulter, R. Collins, and P. Sever. Adverse events associated with unblinded, but not with blinded, statin therapy in the Anglo-Scandinavian cardiac outcomes trial—lipid-lowering arm (ASCOT-LLA): a randomised double-blind placebo-controlled trial and its non-randomised non-blind extension phase. Lancet 389:2473–2481, 2017.PubMedCrossRefGoogle Scholar
  59. 59.
    Gyemant, G., A. Zajacz, B. Becsi, C. Ragunath, N. Ramasubbu, F. Erdodi, G. Batta, and L. Kandra. Evidence for pentagalloyl glucose binding to human salivary alpha-amylase through aromatic amino acid residues. Biochim. Biophys. Acta 1794:291–296, 2009.PubMedCrossRefGoogle Scholar
  60. 60.
    Hagerman, A. E., M. E. Rice, and N. T. Ritchard. Mechanisms of protein precipitation for two tannins, pentagalloyl glucose and epicatechin16(4 → 8) catechin (procyanidin). J. Agric. Food Chem. 46:2590–2595, 1998.CrossRefGoogle Scholar
  61. 61.
    Heath, C. H., A. Sorace, J. Knowles, E. Rosenthal, and K. Hoyt. Microbubble therapy enhances anti-tumor properties of cisplatin and cetuximab in vitro and in vivo. Otolaryngol. Head Neck Surg. 146:938–945, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Ho, L.-L., W.-J. Chen, S.-Y. Lin-Shiau, and J.-K. Lin. Penta-O-galloyl-β-d-glucose inhibits the invasion of mouse melanoma by suppressing metalloproteinase-9 through down-regulation of activator protein-1. Eur. J. Pharmacol. 453:149–158, 2002.PubMedCrossRefGoogle Scholar
  63. 63.
    Hoff, L., Sontum, P. C., and Hoff, B. Acoustic properties of shell-encapsulated, gas-filled ultrasound contrast agents. In: 1996 IEEE US Symp. IEEE, 1996, pp. 1441–1444.Google Scholar
  64. 64.
    Hofmann, T., A. Glabasnia, B. Schwarz, K. N. Wisman, K. A. Gangwer, and A. E. Hagerman. Protein binding and astringent taste of a polymeric procyanidin, 1,2,3,4,6-penta-O-galloyl-beta-d-glucopyranose, castalagin, and grandinin. J. Agric. Food Chem. 54:9503–9509, 2006.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Hofmann, T., E. Nebehaj, and L. Albert. Antioxidant properties and detailed polyphenol profiling of European hornbeam (Carpinus betulus L.) leaves by multiple antioxidant capacity assays and high-performance liquid chromatography/multistage electrospray mass spectrometry. Ind. Crops Prod. 87:340–349, 2016.CrossRefGoogle Scholar
  66. 66.
  67. 67.
    Huh, J. E., E. O. Lee, M. S. Kim, K. S. Kang, C. H. Kim, B. C. Cha, Y. J. Surh, and S. H. Kim. Penta-O-galloyl-beta-d-glucose suppresses tumor growth via inhibition of angiogenesis and stimulation of apoptosis: roles of cyclooxygenase-2 and mitogen-activated protein kinase pathways. Carcinogenesis 26:1436–1445, 2005.PubMedCrossRefGoogle Scholar
  68. 68.
    Isenburg, J. C., N. V. Karamchandani, D. T. Simionescu, and N. R. Vyavahare. Structural requirements for stabilization of vascular elastin by polyphenolic tannins. Biomaterials 27:3645–3651, 2006.PubMedGoogle Scholar
  69. 69.
    Isenburg, J. C., Ogle, M. F. Compositions for tissue stabilization. http://www.google.la/patents/US20160136109. Google Patents, 2016.
  70. 70.
    Isenburg, J. C., D. T. Simionescu, B. C. Starcher, and N. R. Vyavahare. Elastin stabilization for treatment of abdominal aortic aneurysms. Circulation 115:1729–1737, 2007.PubMedCrossRefGoogle Scholar
  71. 71.
    Isenburg, J. C., D. T. Simionescu, and N. R. Vyavahare. Elastin stabilization in cardiovascular implants: improved resistance to enzymatic degradation by treatment with tannic acid. Biomaterials 25:3293–3302, 2004.PubMedCrossRefGoogle Scholar
  72. 72.
    Isenburg, J. C., D. T. Simionescu, and N. R. Vyavahare. Tannic acid treatment enhances biostability and reduces calcification of glutaraldehyde fixed aortic wall. Biomaterials 26:1237–1245, 2005.PubMedCrossRefGoogle Scholar
  73. 73.
    Isenburg, J. C., Vyavahare, N. R., Ogle, M. F. Treatment of aneurysm with application of connective tissue stabilization agent in combination with a delivery vehicle. http://www.google.bs/patents/US20090214654. Google Patents, 2009.
  74. 74.
    Jablonowski, L. J., D. Conover, N. T. Teraphongphom, and M. A. Wheatley. Manipulating multifaceted microbubble shell composition to target both TRAIL-sensitive and resistant cells. J. Biomed. Mater. Res. A 106:1903–1915, 2018.PubMedCrossRefGoogle Scholar
  75. 75.
    Jang, S. E., S. R. Hyam, J. J. Jeong, M. J. Han, and D. H. Kim. Penta-O-galloyl-beta-d-glucose ameliorates inflammation by inhibiting MyD88/NF-kappaB and MyD88/MAPK signalling pathways. Br. J. Pharmacol. 170:1078–1091, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Jeon, W. K., J. H. Lee, H. K. Kim, A. Y. Lee, S. O. Lee, Y. S. Kim, S. Y. Ryu, S. Y. Kim, Y. J. Lee, and B. S. Ko. Anti-platelet effects of bioactive compounds isolated from the bark of Rhus verniciflua Stokes. J. Ethnopharmacol. 106:62–69, 2006.PubMedCrossRefGoogle Scholar
  77. 77.
    Jiamboonsri, P., P. Pithayanukul, R. Bavovada, J. Leanpolchareanchai, T. Yin, S. Gao, and M. Hu. Factors influencing oral bioavailability of thai mango seed kernel extract and its key phenolic principles. Molecules 20:21254–21273, 2015.PubMedCrossRefGoogle Scholar
  78. 78.
    Kageyama-Yahara, N., Y. Suehiro, F. Maeda, S. Kageyama, J. Fukuoka, T. Katagiri, T. Yamamoto, and M. Kadowaki. Pentagalloylglucose down-regulates mast cell surface FcepsilonRI expression in vitro and in vivo. FEBS Lett. 584:111–118, 2010.PubMedCrossRefGoogle Scholar
  79. 79.
    Kang, D. G., M. K. Moon, D. H. Choi, J. K. Lee, T. O. Kwon, and H. S. Lee. Vasodilatory and anti-inflammatory effects of the 1,2,3,4,6-penta-O-galloyl-beta-d-glucose (PGG) via a nitric oxide-cGMP pathway. Eur. J. Pharmacol. 524:111–119, 2005.PubMedCrossRefGoogle Scholar
  80. 80.
    Kanoh, R., T. Hatano, H. Ito, T. Yoshida, and M. Akagi. Effects of tannins and related polyphenols on superoxide-induced histamine release from rat peritoneal mast cells. Phytomedicine 7:297–302, 2000.PubMedCrossRefGoogle Scholar
  81. 81.
    Karrowni, W., S. Dughman, G. P. Hajj, and F. J. Miller, Jr. Statin therapy reduces growth of abdominal aortic aneurysms. J. Invest. Med. 59:1239–1243, 2011.CrossRefGoogle Scholar
  82. 82.
    Kim, W., R. T. Gandhi, C. S. Pena, R. E. Herrera, M. B. Schernthaner, J. M. Acuna, V. N. Becerra, and B. T. Katzen. Influence of statin therapy on aneurysm sac regression after endovascular aortic repair. J. Vasc. Interv. Radiol. 28:35–43, 2017.PubMedCrossRefGoogle Scholar
  83. 83.
    Kim, S. J., S. A. Sancheti, S. S. Sancheti, B. H. Um, S. M. Yu, and S. Y. Seo. Effect of 1,2,3,4,6-penta-O-galloyl-beta-d-glucose on elastase and hyaluronidase activities and its type II collagen expression. Acta Pol. Pharm. 67:145–150, 2010.PubMedGoogle Scholar
  84. 84.
    Kim, Y. H., M. Yoshimoto, K. Nakayama, S. Tanino, Y. Fujimura, K. Yamada, and H. Tachibana. Tannic acid, a higher galloylated pentagalloylglucose, suppresses antigen-specific IgE production by inhibiting varepsilon germline transcription induced by STAT6 activation. FEBS Open Bio. 3:341–345, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Kiss, A., B. Becsi, B. Kolozsvari, I. Komaromi, K. E. Kover, and F. Erdodi. Epigallocatechin-3-gallate and penta-O-galloyl-beta-d-glucose inhibit protein phosphatase-1. FEBS J. 280:612–626, 2013.PubMedCrossRefGoogle Scholar
  86. 86.
    Kiss, A. K., A. Filipek, B. Zyzynska-Granica, and M. Naruszewicz. Effects of penta-O-galloyl-beta-d-glucose on human neutrophil function: significant down-regulation of L-selectin expression. Phytother. Res. 27:986–992, 2013.PubMedCrossRefGoogle Scholar
  87. 87.
    Klibanov, A. L. Ligand-carrying gas-filled microbubbles: ultrasound contrast agents for targeted molecular imaging. Bioconjug. Chem. 16:9–17, 2005.PubMedCrossRefGoogle Scholar
  88. 88.
    Kloster, B. O., L. Lund, and J. S. Lindholt. Inhibition of early AAA formation by aortic intraluminal pentagalloyl glucose (PGG) infusion in a novel porcine AAA model. Ann. Med. Surg. 7:65–70, 2016.CrossRefGoogle Scholar
  89. 89.
    Kooiman, K., H. J. Vos, M. Versluis, and N. de Jong. Acoustic behavior of microbubbles and implications for drug delivery. Adv. Drug Deliv. Rev. 72:28–48, 2014.PubMedCrossRefGoogle Scholar
  90. 90.
    Krook, M. A., and A. E. Hagerman. Stability of polyphenols epigallocatechin gallate and pentagalloyl glucose in a simulated digestive system. Food Res. Int. 49:112–116, 2012.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Kuo, P. T., T. P. Lin, L. C. Liu, C. H. Huang, J. K. Lin, J. Y. Kao, and T. D. Way. Penta-O-galloyl-beta-d-glucose suppresses prostate cancer bone metastasis by transcriptionally repressing EGF-induced MMP-9 expression. J. Agric. Food Chem. 57:3331–3339, 2009.PubMedCrossRefGoogle Scholar
  92. 92.
    Larrosa, M., M. T. Garcia-Conesa, J. C. Espin, and F. A. Tomas-Barberan. Ellagitannins, ellagic acid and vascular health. Mol. Aspects Med. 31:513–539, 2010.PubMedCrossRefGoogle Scholar
  93. 93.
    Lederle, F. A., G. R. Johnson, S. E. Wilson, E. P. Chute, F. N. Littooy, D. Bandyk, W. C. Krupski, G. W. Barone, C. W. Acher, and D. J. Ballard. Prevalence and associations of abdominal aortic aneurysm detected through screening. Ann. Intern. Med. 126:441, 1997.PubMedCrossRefGoogle Scholar
  94. 94.
    Lee, H. J., N. J. Seo, S. J. Jeong, Y. Park, D. B. Jung, W. Koh, H. J. Lee, E. O. Lee, K. S. Ahn, K. S. Ahn, J. Lu, and S. H. Kim. Oral administration of penta-O-galloyl-beta-d-glucose suppresses triple-negative breast cancer xenograft growth and metastasis in strong association with JAK1-STAT3 inhibition. Carcinogenesis 32:804–811, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Lee, E. H., D. G. Song, J. Y. Lee, C. H. Pan, B. H. Um, and S. H. Jung. Inhibitory effect of the compounds isolated from Rhus verniciflua on aldose reductase and advanced glycation endproducts. Biol. Pharm. Bull. 31:1626–1630, 2008.PubMedCrossRefGoogle Scholar
  96. 96.
    Lentacker, I., S. C. De Smedt, and N. N. Sanders. Drug loaded microbubble design for ultrasound triggered delivery. Soft Matter 5:2161–2170, 2009.CrossRefGoogle Scholar
  97. 97.
    Li, L., A. A. Shaik, J. Zhang, K. Nhkata, L. Wang, Y. Zhang, C. Xing, S. H. Kim, and J. Lu. Preparation of penta-O-galloyl-beta-d-glucose from tannic acid and plasma pharmacokinetic analyses by liquid-liquid extraction and reverse-phase HPLC. J. Pharm. Biomed. Anal. 54:545–550, 2011.PubMedCrossRefGoogle Scholar
  98. 98.
    Lin, T. C., F. L. Hsu, and J. T. Cheng. Antihypertensive activity of corilagin and chebulinic acid, tannins from lumnitzera-racemosa. J. Nat. Prod. 56:629–632, 1993.CrossRefGoogle Scholar
  99. 99.
    Lindeman, J. H., B. A. Ashcroft, J. W. Beenakker, M. van Es, N. B. Koekkoek, F. A. Prins, J. F. Tielemans, H. Abdul-Hussien, R. A. Bank, and T. H. Oosterkamp. Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome. Proc. Natl. Acad. Sci. USA 107:862–865, 2010.PubMedCrossRefGoogle Scholar
  100. 100.
    Liu, J. C., F. L. Hsu, J. C. Tsai, P. Chan, J. Y. Liu, G. N. Thomas, B. Tomlinson, M. Y. Lo, and J. Y. Lin. Antihypertensive effects of tannins isolated from traditional Chinese herbs as non-specific inhibitors of angiontensin converting enzyme. Life Sci. 73:1543–1555, 2003.PubMedCrossRefGoogle Scholar
  101. 101.
    Lopez-de-Andres, A., I. Jimenez-Trujillo, R. Jimenez-Garcia, V. Hernandez-Barrera, J. M. de Miguel-Yanes, M. Mendez-Bailon, N. Perez-Farinos, M. A. Salinero-Fort, and P. Carrasco-Garrido. National trends in incidence and outcomes of abdominal aortic aneurysm among elderly type 2 diabetic and non-diabetic patients in Spain (2003–2012). Cardiovasc. Diabetol. 14:48, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Ma, C. X., X. Zhao, P. Wang, P. Jia, X. F. Zhao, C. N. Xiao, and X. H. Zheng. Metabolite characterization of penta-O-galloyl-beta-d-glucose in rat biofluids by HPLC-QTOF-MS. Chin. Herb. Med. 10:73–79, 2018.CrossRefGoogle Scholar
  103. 103.
    Manach, C., A. Scalbert, C. Morand, C. Remesy, and L. Jimenez. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79:727–747, 2004.PubMedCrossRefGoogle Scholar
  104. 104.
    Mao, X., C. Gu, D. Chen, B. Yu, and J. He. Oxidative stress-induced diseases and tea polyphenols. Oncotarget 8:81649–81661, 2017.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Martufi, G., E. S. Di Martino, C. H. Amon, S. C. Muluk, and E. A. Finol. Three-dimensional geometrical characterization of abdominal aortic aneurysms: image-based wall thickness distribution. J. Biomech. Eng. 131:061015, 2009.PubMedCrossRefGoogle Scholar
  106. 106.
    Meijer, C. A., T. Stijnen, M. N. Wasser, J. F. Hamming, J. H. van Bockel, J. H. Lindeman, and G. Pharmaceutical Aneurysm Stabilisation Trial Study. Doxycycline for stabilization of abdominal aortic aneurysms: a randomized trial. Ann. Intern. Med. 159:815–823, 2013.PubMedCrossRefGoogle Scholar
  107. 107.
    Mendonca, P., E. Taka, D. Bauer, M. Cobourne-Duval, and K. F. Soliman. The attenuating effects of 1,2,3,4,6 penta-O-galloyl-beta-d-glucose on inflammatory cytokines release from activated BV-2 microglial cells. J. Neuroimmunol. 305:9–15, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Mercuri, J. J., S. Patnaik, G. Dion, S. S. Gill, J. Liao, and D. T. Simionescu. Regenerative potential of decellularized porcine nucleus pulposus hydrogel scaffolds: stem cell differentiation, matrix remodeling, and biocompatibility studies. Tissue Eng. A 19:952–966, 2013.CrossRefGoogle Scholar
  109. 109.
    Miyake, T., and R. Morishita. Pharmacological treatment of abdominal aortic aneurysm. Cardiovasc. Res. 83:436–443, 2009.PubMedCrossRefGoogle Scholar
  110. 110.
    Mohamed, F., P. Marchettini, O. A. Stuart, and P. H. Sugarbaker. Pharmacokinetics and tissue distribution of intraperitoneal paclitaxel with different carrier solutions. Cancer Chemother. Pharmacol. 52:405–410, 2003.PubMedCrossRefGoogle Scholar
  111. 111.
    Mohan, C. G., G. L. Viswanatha, G. Savinay, C. E. Rajendra, and P. D. Halemani. 1,2,3,4,6 penta-O-galloyl-beta-d-glucose, a bioactivity guided isolated compound from Mangifera indica inhibits 11beta-HSD-1 and ameliorates high fat diet-induced diabetes in C57BL/6 mice. Phytomedicine 20:417–426, 2013.PubMedCrossRefGoogle Scholar
  112. 112.
    Moran, C. S., S. W. Seto, S. M. Krishna, S. Sharma, R. J. Jose, E. Biros, Y. Wang, S. K. Morton, and J. Golledge. Parenteral administration of factor Xa/IIa inhibitors limits experimental aortic aneurysm and atherosclerosis. Sci. Rep. 7:43079, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Moris, D., E. Mantonakis, E. Avgerinos, M. Makris, C. Bakoyiannis, E. Pikoulis, and S. Georgopoulos. Novel biomarkers of abdominal aortic aneurysm disease: identifying gaps and dispelling misperceptions. BioMed Res. Int. 2014:925840, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Moro, F., I. De Blasis, B. Virgilio, A. Di Legge, G. Rindi, L. Bonomo, M. Storto, and A. C. Testa. P27.02: first in human study using KDR-targeted microbubbles (BR55) ultrasound molecular imaging in ovarian masses. Ultrasound Obstet. Gynecol. 48:255, 2016.CrossRefGoogle Scholar
  115. 115.
    Mosorin, M., J. Juvonen, F. Biancari, J. Satta, H. M. Surcel, M. Leinonen, P. Saikku, and T. Juvonen. Use of doxycycline to decrease the growth rate of abdominal aortic aneurysms: a randomized, double-blind, placebo-controlled pilot study. J. Vasc. Surg. 34:606–610, 2001.PubMedCrossRefGoogle Scholar
  116. 116.
    Murphy, M. P. Safety and efficacy of allogeneic MSCs in promoting T-regulatory cells in patients with small abdominal aortic aneurysms. http://www.clinicaltrial.co/ShowTrial/NCT02846883, 2016.
  117. 117.
    Nesbitt, W. S., E. Westein, F. J. Tovar-Lopez, E. Tolouei, A. Mitchell, J. Fu, J. Carberry, A. Fouras, and S. P. Jackson. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat. Med. 15:665–673, 2009.PubMedCrossRefGoogle Scholar
  118. 118.
    Neveu, V., J. Perez-Jimenez, F. Vos, V. Crespy, L. du Chaffaut, L. Mennen, C. Knox, R. Eisner, J. Cruz, D. Wishart, and A. Scalbert. Phenol-explorer: an online comprehensive database on polyphenol contents in foods. Database 2010:bap024, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Nosoudi, N., A. Chowdhury, S. Siclari, S. Karamched, V. Parasaram, J. Parrish, P. Gerard, and N. Vyavahare. Reversal of vascular calcification and aneurysms in a rat model using dual targeted therapy with EDTA- and PGG-loaded nanoparticles. Theranostics 6:1975–1987, 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Nosoudi, N., A. Chowdhury, S. Siclari, V. Parasaram, S. Karamched, and N. Vyavahare. Systemic delivery of nanoparticles loaded with pentagalloyl glucose protects elastic lamina and prevents abdominal aortic aneurysm in rats. J. Cardiovasc. Transl. Res. 9:445–455, 2016.PubMedCrossRefGoogle Scholar
  121. 121.
    Oh, G. S., H. O. Pae, B. M. Choi, H. S. Lee, I. K. Kim, Y. G. Yun, J. D. Kim, and H. T. Chung. Penta-O-galloyl-beta-d-glucose inhibits phorbol myristate acetate-induced interleukin-8 [correction of intereukin-8] gene expression in human monocytic U937 cells through its inactivation of nuclear factor-kappaB. Int. Immunopharmacol. 4:377–386, 2004.PubMedCrossRefGoogle Scholar
  122. 122.
    Paefgen, V., D. Doleschel, and F. Kiessling. Evolution of contrast agents for ultrasound imaging and ultrasound-mediated drug delivery. Front. Pharmacol. 6:197, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Pan, M. H., S. Y. Lin-Shiau, C. T. Ho, J. H. Lin, and J. K. Lin. Suppression of lipopolysaccharide-induced nuclear factor-kappaB activity by theaflavin-3,3′-digallate from black tea and other polyphenols through down-regulation of IkappaB kinase activity in macrophages. Biochem. Pharmacol. 59:357–367, 2000.PubMedCrossRefGoogle Scholar
  124. 124.
    Parasaram, V., N. Nosoudi, A. Chowdhury, and N. Vyavahare. Pentagalloyl glucose increases elastin deposition, decreases reactive oxygen species and matrix metalloproteinase activity in pulmonary fibroblasts under inflammatory conditions. Biochem. Biophys. Res. Commun. 499:24–29, 2018.PubMedCrossRefGoogle Scholar
  125. 125.
    Parikh, S. A., R. Gomez, M. Thirugnanasambandam, S. S. Chauhan, V. De Oliveira, S. C. Muluk, M. K. Eskandari, and E. V. Finol. Decision tree based classification of abdominal aortic aneurysms using geometry quantification measures. Ann. Biomed. Eng. 2018.  https://doi.org/10.1007/s10439-018-02116-w.PubMedCrossRefGoogle Scholar
  126. 126.
    Park, J. K., H. J. Cho, Y. Lim, Y. H. Cho, and C. H. Lee. Hypocholestrolemic effect of CJ90002 in hamsters: a potent inhibitor for squalene synthase from Paeonia moutan. J. Microbiol. Biotechnol. 12:222–227, 2002.Google Scholar
  127. 127.
    Park, E., N. H. Lee, J. S. Baik, and Y. Jee. Elaeocarpus sylvestris modulates gamma-ray-induced immunosuppression in mice: implications in radioprotection. Phytother. Res. 22:1046–1051, 2008.PubMedCrossRefGoogle Scholar
  128. 128.
    Parkinson, F., S. Ferguson, P. Lewis, I. M. Williams, C. P. Twine, and N South East Wales Vascular. Rupture rates of untreated large abdominal aortic aneurysms in patients unfit for elective repair. J. Vasc. Surg. 61:1606–1612, 2015.PubMedCrossRefGoogle Scholar
  129. 129.
    Pennel, T., G. Fercana, D. Bezuidenhout, A. Simionescu, T. H. Chuang, P. Zilla, and D. Simionescu. The performance of cross-linked acellular arterial scaffolds as vascular grafts; pre-clinical testing in direct and isolation loop circulatory models. Biomaterials 35:6311–6322, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Phillips, E. H., A. A. Yrineo, H. D. Schroeder, K. E. Wilson, J. X. Cheng, and C. J. Goergen. Morphological and biomechanical differences in the elastase and AngII apoE(−/−) rodent models of abdominal aortic aneurysms. BioMed Res. Int. 2015:413189, 2015.PubMedPubMedCentralGoogle Scholar
  131. 131.
    Piao, M. J., K. A. Kang, R. Zhang, D. O. Ko, Z. H. Wang, K. H. Lee, W. Y. Chang, S. Chae, Y. Jee, T. Shin, J. W. Park, N. H. Lee, and J. W. Hyun. Antioxidant properties of 1,2,3,4,6-penta-O-galloyl-β-d-glucose from Elaeocarpus sylvestris var. ellipticus. Food Chem. 115:412–418, 2009.CrossRefGoogle Scholar
  132. 132.
    Pintea, A., D. Rugină, and Z. Diaconeasa. 4-Pharmacologically active plant-derived natural products. In: Smart Nanoparticles for Biomedicine, edited by G. Ciofani. Amsterdam: Elsevier, 2018, pp. 49–64.CrossRefGoogle Scholar
  133. 133.
    Pitt, W. G., G. A. Husseini, and B. J. Staples. Ultrasonic drug delivery—a general review. Exp. Opin. Drug Deliv. 1:37–56, 2004.CrossRefGoogle Scholar
  134. 134.
    Prall, A. K., G. M. Longo, W. G. Mayhan, E. A. Waltke, B. Fleckten, R. W. Thompson, and B. T. Baxter. Doxycycline in patients with abdominal aortic aneurysms and in mice: comparison of serum levels and effect on aneurysm growth in mice. J. Vasc. Surg. 35:923–929, 2002.PubMedCrossRefGoogle Scholar
  135. 135.
    Rader, D. J. High-density lipoproteins and atherosclerosis. Am. J. Cardiol. 90:62i–70i, 2002.PubMedCrossRefGoogle Scholar
  136. 136.
    Ragheb, A. O., Ruane, P. H., and Biggs, D. P. Delivery of elastin-stabilizing compound within a body lumen. https://www.google.com/patents/WO2007133479A2?cl=en. Google Patents, 2007.
  137. 137.
    Ramakrishnan, S., K. Dharmalingam, S. T. Panchanatham, and S. Palanivelu. Efficacy of tridham and 1,2,3,4,6-penta-O-galloyl-β-d-glucose in reversing lipid peroxidation levels and mitochondrial antioxidant status in 7,12-dimethylbenzeneanthracene (Dmba) induced breast cancer in Sprague–Dawley rats. Int. J. Pharm. Pharm. Sci. 8:288, 2016.CrossRefGoogle Scholar
  138. 138.
    Ramaswamy, A. K., M. Hamilton, 2nd, R. V. Joshi, B. P. Kline, R. Li, P. Wang, and C. J. Goergen. Molecular imaging of experimental abdominal aortic aneurysms. Sci. World J. 2013:973150, 2013.CrossRefGoogle Scholar
  139. 139.
    Raut, S., S. Chandra, J. Shum, C. B. Washington, S. C. Muluk, E. A. Finol, and J. F. Rodriguez. Biological, geometric and biomechanical factors influencing abdominal aortic aneurysm rupture risk: a comprehensive review. Recent Patents Med. Imaging 3:44–59, 2013.CrossRefGoogle Scholar
  140. 140.
    Ren, Y., and X. Chen. Distribution, bioactivities and therapeutical potentials of pentagalloylglucopyranose. Curr. Bioact. Compd. 3:81–89, 2007.CrossRefGoogle Scholar
  141. 141.
    Ren, Y., K. Himmeldirk, and X. Chen. Synthesis and structure-activity relationship study of antidiabetic penta-O-galloyl-d-glucopyranose and its analogues. J. Med. Chem. 49:2829–2837, 2006.PubMedCrossRefGoogle Scholar
  142. 142.
    Ruggeri, Z. M., J. N. Orje, R. Habermann, A. B. Federici, and A. J. Reininger. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108:1903–1910, 2006.PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Ryan, S. M., G. Mantovani, X. Wang, D. M. Haddleton, and D. J. Brayden. Advances in PEGylation of important biotech molecules: delivery aspects. Exp. Opin. Drug Deliv. 5:371–383, 2008.CrossRefGoogle Scholar
  144. 144.
    Safar, M. E., B. I. Levy, and H. Struijker-Boudier. Current perspectives on arterial stiffness and pulse pressure in hypertension and cardiovascular diseases. Circulation 107:2864–2869, 2003.PubMedCrossRefGoogle Scholar
  145. 145.
    Salata, K., M. Syed, M. Hussain, N. Alsaif, S. Verma, and M. Al-Omran. The impact of statins on abdominal aortic aneurysm growth, rupture, and perioperative outcomes: a systematic review and meta-analysis. J. Vasc. Surg. 66:E66–E67, 2017.CrossRefGoogle Scholar
  146. 146.
    Sanna, V., G. Lubinu, P. Madau, N. Pala, S. Nurra, A. Mariani, and M. Sechi. Polymeric nanoparticles encapsulating white tea extract for nutraceutical application. J. Agric. Food Chem. 63:2026–2032, 2015.PubMedCrossRefGoogle Scholar
  147. 147.
    Sanna, V., A. M. Roggio, A. M. Posadino, A. Cossu, S. Marceddu, A. Mariani, V. Alzari, S. Uzzau, G. Pintus, and M. Sechi. Novel docetaxel-loaded nanoparticles based on poly(lactide-co-caprolactone) and poly(lactide-co-glycolide-co-caprolactone) for prostate cancer treatment: formulation, characterization, and cytotoxicity studies. Nanoscale Res. Lett. 6:260, 2011.PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Schriefl, A. J., G. Zeindlinger, D. M. Pierce, P. Regitnig, and G. A. Holzapfel. Determination of the layer-specific distributed collagen fibre orientations in human thoracic and abdominal aortas and common iliac arteries. J. R. Soc. Interface 9:1275–1286, 2012.PubMedCrossRefGoogle Scholar
  149. 149.
    Schroff, P., C. M. Gamboa, R. W. Durant, A. Oikeh, J. S. Richman, and M. M. Safford. Vulnerabilities to Health disparities and statin use in the REGARDS (reasons for geographic and racial differences in stroke) study. J. Am. Heart Assoc. 6:e005449, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Shavandi, A., A. E. A. Bekhit, P. Saeedi, Z. Izadifar, A. A. Bekhit, and A. Khademhosseini. Polyphenol uses in biomaterials engineering. Biomaterials 167:91–106, 2018.PubMedCrossRefGoogle Scholar
  151. 151.
    Shen, A. M. Subcutaneous delivery of protein therapeutics https://search.proquest.com/docview/2003275315. Rutgers University-Graduate School-New Brunswick, 2017.
  152. 152.
    Shimada, T. Salivary proteins as a defense against dietary tannins. J. Chem. Ecol. 32:1149–1163, 2006.PubMedCrossRefGoogle Scholar
  153. 153.
    Shum, J., G. Martufi, E. Di Martino, C. B. Washington, J. Grisafi, S. C. Muluk, and E. A. Finol. Quantitative assessment of abdominal aortic aneurysm geometry. Ann. Biomed. Eng. 39:277–286, 2011.PubMedCrossRefGoogle Scholar
  154. 154.
    Sierad, L. N., A. Simionescu, C. Albers, J. Chen, J. Maivelett, M. E. Tedder, J. Liao, and D. T. Simionescu. Design and testing of a pulsatile conditioning system for dynamic endothelialization of polyphenol-stabilized tissue engineered heart valves. Cardiovasc. Eng. Technol. 1:138–153, 2010.PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Sillesen, H., N. Eldrup, R. Hultgren, J. Lindeman, K. Bredahl, M. Thompson, A. Wanhainen, U. Wingren, J. Swedenborg, and A. T. Investigators. Randomized clinical trial of mast cell inhibition in patients with a medium-sized abdominal aortic aneurysm. Br. J. Surg. 102:894–901, 2015.PubMedCrossRefGoogle Scholar
  156. 156.
    Sinha, A., N. Nosoudi, and N. Vyavahare. Elasto-regenerative properties of polyphenols. Biochem. Biophys. Res. Commun. 444:205–211, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Sinha, A., A. Shaporev, N. Nosoudi, Y. Lei, A. Vertegel, S. Lessner, and N. Vyavahare. Nanoparticle targeting to diseased vasculature for imaging and therapy. Nanomedicine 10:1003–1012, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Sirsi, S., and M. Borden. Microbubble compositions, properties and biomedical applications. Bubble Sci. Eng. Technol. 1:3–17, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Sirsi, S. R., and M. A. Borden. State-of-the-art materials for ultrasound-triggered drug delivery. Adv. Drug Deliv. Rev. 72:3–14, 2014.PubMedCrossRefGoogle Scholar
  160. 160.
    Sirsi, S. R., C. Fung, S. Garg, M. Y. Tianning, P. A. Mountford, and M. A. Borden. Lung surfactant microbubbles increase lipophilic drug payload for ultrasound-targeted delivery. Theranostics 3:409–419, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    Skopec, M. M., A. E. Hagerman, and W. H. Karasov. Do salivary proline-rich proteins counteract dietary hydrolyzable tannin in laboratory rats? J. Chem. Ecol. 30:1679–1692, 2004.PubMedCrossRefGoogle Scholar
  162. 162.
    Sorace, A. G., M. Korb, J. M. Warram, H. Umphrey, K. R. Zinn, E. Rosenthal, and K. Hoyt. Ultrasound-stimulated drug delivery for treatment of residual disease after incomplete resection of head and neck cancer. Ultrasound Med. Biol. 40:755–764, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Sugatani, J., N. Fukazawa, K. Ujihara, K. Yoshinari, I. Abe, H. Noguchi, and M. Miwa. Tea polyphenols inhibit acetyl-CoA:1-alkyl-<i>sn</i>-glycero-3-phosphocholine acetyltransferase (a key enzyme in platelet-activating factor biosynthesis) and platelet-activating factor-induced platelet aggregation. Int. Arch. Allergy Immunol. 134:17–28, 2004.PubMedCrossRefGoogle Scholar
  164. 164.
    Swart, A. M., S. Burdett, J. Ledermann, P. Mook, and M. K. Parmar. Why i.p. therapy cannot yet be considered as a standard of care for the first-line treatment of ovarian cancer: a systematic review. Ann. Oncol. 19:688–695, 2008.PubMedCrossRefGoogle Scholar
  165. 165.
    Sweeting, M. J., S. G. Thompson, L. C. Brown, J. T. Powell, and R. collaborators. Meta-analysis of individual patient data to examine factors affecting growth and rupture of small abdominal aortic aneurysms. Br. J. Surg. 99:655–665, 2012.PubMedCrossRefGoogle Scholar
  166. 166.
    Takagi, H., H. Manabe, N. Kawai, S. N. Goto, and T. Umemoto. Serum high-density and low-density lipoprotein cholesterol is associated with abdominal aortic aneurysm presence: a systematic review and meta-analysis. Int. Angiol. 29:371–375, 2010.PubMedGoogle Scholar
  167. 167.
    Tam, H., W. Zhang, K. R. Feaver, N. Parchment, M. S. Sacks, and N. Vyavahare. A novel crosslinking method for improved tear resistance and biocompatibility of tissue based biomaterials. Biomaterials 66:83–91, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Tam, H., W. Zhang, D. Infante, N. Parchment, M. Sacks, and N. Vyavahare. Fixation of bovine pericardium-based tissue biomaterial with irreversible chemistry improves biochemical and biomechanical properties. J. Cardiovasc. Transl. Res. 10:194–205, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  169. 169.
    Tanios, F., M. W. Gee, J. Pelisek, S. Kehl, J. Biehler, V. Grabher-Meier, W. A. Wall, H. H. Eckstein, and C. Reeps. Interaction of biomechanics with extracellular matrix components in abdominal aortic aneurysm wall. Eur. J. Vasc. Endovasc. Surg. 50:167–174, 2015.PubMedCrossRefGoogle Scholar
  170. 170.
    Tedder, M. E., J. Liao, B. Weed, C. Stabler, H. Zhang, A. Simionescu, and D. T. Simionescu. Stabilized collagen scaffolds for heart valve tissue engineering. Tissue Eng. A 15:1257–1268, 2009.CrossRefGoogle Scholar
  171. 171.
    Tedder, M. E., A. Simionescu, J. Chen, J. Liao, and D. T. Simionescu. Assembly and testing of stem cell-seeded layered collagen constructs for heart valve tissue engineering. Tissue Eng. A 17:25–36, 2011.CrossRefGoogle Scholar
  172. 172.
    Thirugnanasambandam, M., D. Simionescu, G. P. Escobar, E. A. Sprague, B. Goins, G. Clarke, H. Han, K. Amezcua, O. Adeyinka, C. Goergen, and E. A. Finol. The effect of pentagalloyl glucose on the wall mechanics and inflammatory activity of rat abdominal aortic aneurysms. J. Biomech. Eng. 140:8, 2018.CrossRefGoogle Scholar
  173. 173.
    Thomasset, S. C., D. P. Berry, G. Garcea, T. Marczylo, W. P. Steward, and A. J. Gescher. Dietary polyphenolic phytochemicals–promising cancer chemopreventive agents in humans? A review of their clinical properties. Int. J. Cancer 120:451–458, 2007.PubMedCrossRefGoogle Scholar
  174. 174.
    Thompson, R. W., and B. T. Baxter. MMP inhibition in abdominal aortic aneurysms. Rationale for a prospective randomized clinical trial. Ann N Y Acad Sci 878:159–178, 1999.PubMedCrossRefGoogle Scholar
  175. 175.
    Toda, M., J. Kawabata, and T. Kasai. Inhibitory effects of ellagi- and gallotannins on rat intestinal alpha-glucosidase complexes. Biosci. Biotechnol. Biochem. 65:542–547, 2001.PubMedCrossRefGoogle Scholar
  176. 176.
    Torres-Leon, C., J. Ventura-Sobrevilla, L. Serna-Cock, J. A. Ascacio-Valdes, J. Contreras-Esquivel, and C. N. Aguilar. Pentagalloylglucose (PGG): a valuable phenolic compound with functional properties. J. Funct. Foods 37:176–189, 2017.CrossRefGoogle Scholar
  177. 177.
    Tripi, D. R., and N. R. Vyavahare. Neomycin and pentagalloyl glucose enhanced cross-linking for elastin and glycosaminoglycans preservation in bioprosthetic heart valves. J. Biomater. Appl. 28:757–766, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  178. 178.
    Tu, Z., W. Gong, Y. Zhang, Y. Feng, Y. Liu, and C. Tu. Inhibition of rabies virus by 1,2,3,4,6-penta-O-galloyl-beta-d-glucose involves mTOR-dependent autophagy. Viruses 10:201, 2018.PubMedCentralCrossRefGoogle Scholar
  179. 179.
    Vallianou, N. G., A. Kostantinou, M. Kougias, and C. Kazazis. Statins and cancer. Anti-cancer Agents Med. Chem. 14:706–712, 2014.CrossRefGoogle Scholar
  180. 180.
    Venancio, V. P., H. Kim, M. A. Sirven, C. D. Tekwe, G. Honvoh, S. T. Talcott, and S. Mertens-Talcott. Polyphenol-rich Mango (Mangifera indica L.) Ameliorate Functional Constipation Symptoms in Humans beyond Equivalent Amount of Fiber. Mol. Nutr. Food Res. 62:1701034, 2018.CrossRefGoogle Scholar
  181. 181.
    Vijaynagar, B., M. J. Bown, R. D. Sayers, and E. Choke. Potential role for anti-angiogenic therapy in abdominal aortic aneurysms. Eur. J. Clin. Invest. 43:758–765, 2013.PubMedCrossRefGoogle Scholar
  182. 182.
    Villanueva, F. S., W. R. Wagner, M. A. Vannan, and J. Narula. Targeted ultrasound imaging using microbubbles. Cardiol. Clin. 22:283–298, 2004.PubMedCrossRefGoogle Scholar
  183. 183.
    Viswanatha, G. L., H. Shylaja, and C. G. Mohan. Alleviation of transient global ischemia/reperfusion-induced brain injury in rats with 1,2,3,4,6-penta-O-galloyl-beta-d-glucopyranose isolated from Mangifera indica. Eur. J. Pharmacol. 720:286–293, 2013.PubMedCrossRefGoogle Scholar
  184. 184.
    Vyavahare, N. R., Isenburg, J. C., Simionescu, D. T. Elastin stabilization of connective tissue. http://www.google.al/patents/US7252834. Google Patents, 2007.
  185. 185.
    Wang, X., A. Searle, Y. Chen, and K. Peter. Targeted microbubbles for the delivery of MicroRNA-126: treatment and prevention of abdominal aortic aneurysm. Heart Lung Circul. 26:S63, 2017.CrossRefGoogle Scholar
  186. 186.
    Wang, G. W., J. Song, X. Tan, Y. Zhou, J. Chen, R. Li, L. Qiao, J. Song, C. Wang, and L. Zhang. Structural composition of components of geoherb Moutan Cortex contributes to anti-diabetic nephropathy activity. Oncotarget 2018.  https://doi.org/10.18632/oncotarget.23771.CrossRefPubMedPubMedCentralGoogle Scholar
  187. 187.
    Wanhainen A. The efficacy of ticagrelor on abdominal aortic aneurysm expansion. https://clinicaltrials.gov/show/NCT02070653.
  188. 188.
    Westenburg, H. E., K. J. Lee, S. K. Lee, H. H. Fong, R. B. van Breemen, J. M. Pezzuto, and A. D. Kinghorn. Activity-guided isolation of antioxidative constituents of Cotinus coggygria. J. Nat. Prod. 63:1696–1698, 2000.PubMedCrossRefGoogle Scholar
  189. 189.
    Whitlock, M. C., and W. G. Hundley. Noninvasive imaging of flow and vascular function in disease of the aorta. JACC Cardiovasc. Imaging 8:1094–1106, 2015.PubMedPubMedCentralCrossRefGoogle Scholar
  190. 190.
    Wolinsky, H., and S. Glagov. A lamellar unit of aortic medial structure and function in mammals. Circul. Res. 20:99–111, 1967.CrossRefGoogle Scholar
  191. 191.
    Wroblewski, K., R. Muhandiram, A. Chakrabartty, and A. Bennick. The molecular interaction of human salivary histatins with polyphenolic compounds. Eur. J. Biochem. 268:4384–4397, 2001.PubMedCrossRefGoogle Scholar
  192. 192.
    Wu, J., and X. Ding. Hypotensive and physiological effect of angiotensin converting enzyme inhibitory peptides derived from soy protein on spontaneously hypertensive rats. J. Agric. Food Chem. 49:501–506, 2001.PubMedCrossRefGoogle Scholar
  193. 193.
    Xie, P., L. Cui, Y. Shan, and W. Y. Kang. antithrombotic effect and mechanism of radix paeoniae rubra. BioMed Res. Int. 2017:9475074, 2017.PubMedPubMedCentralGoogle Scholar
  194. 194.
    Xiong, F. Y., Nirupama, S., Sirsi, S. R., Lacko, A., and Hoyt, K. Ultrasound-stimulated drug delivery of reconstituted high-density lipoprotein nanoparticles: Effects of drug concentration on tumor uptake. 2017 IEEE International Ultrasonics Symposium (Ius), pp. 1–4, 2017.Google Scholar
  195. 195.
    Xiong, J., Z. Wu, C. Chen, Y. Wei, and W. Guo. Association between diabetes and prevalence and growth rate of abdominal aortic aneurysms: a meta-analysis. Int. J. Cardiol. 221:484–495, 2016.PubMedCrossRefGoogle Scholar
  196. 196.
    Yeo, Y., T. Ito, E. Bellas, C. B. Highley, R. Marini, and D. S. Kohane. In situ cross-linkable hyaluronan hydrogels containing polymeric nanoparticles for preventing postsurgical adhesions. Ann. Surg. 245:819–824, 2007.PubMedPubMedCentralCrossRefGoogle Scholar
  197. 197.
    Yrineo, A. A., A. R. Adelsperger, A. C. Durkes, M. R. Distasi, S. L. Voytik-Harbin, M. P. Murphy, and C. J. Goergen. Murine ultrasound-guided transabdominal para-aortic injections of self-assembling type I collagen oligomers. J. Control Release 249:53–62, 2017.PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Yuan, B., and J. Rychak. Tumor functional and molecular imaging utilizing ultrasound and ultrasound-mediated optical techniques. Am. J. Pathol. 182:305–311, 2013.PubMedPubMedCentralCrossRefGoogle Scholar
  199. 199.
    Zhang, J., L. Li, S. H. Kim, A. E. Hagerman, and J Lu Anti-cancer. anti-diabetic and other pharmacologic and biological activities of penta-galloyl-glucose. Pharm. Res. 26:2066–2080, 2009.PubMedPubMedCentralCrossRefGoogle Scholar
  200. 200.
    Zhao, W., V. Haller, and A. Ritsch. The polyphenol PGG enhances expression of SR-BI and ABCA1 in J774 and THP-1 macrophages. Atherosclerosis 242:611–617, 2015.PubMedCrossRefGoogle Scholar
  201. 201.
    Zou, L. Q., S. F. Peng, W. Liu, L. Gan, W. L. Liu, R. H. Liang, C. M. Liu, J. Niu, Y. L. Cao, Z. Liu, and X. Chen. Improved in vitro digestion stability of (-)-epigallocatechin gallate through nanoliposome encapsulation. Food Res. Int. 64:492–499, 2014.PubMedCrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2018

Authors and Affiliations

  1. 1.Vascular Biomechanics and Biofluids Laboratory, Department of Mechanical EngineeringThe University of Texas at San AntonioSan AntonioUSA
  2. 2.Department of BioengineeringClemson UniversityClemsonUSA
  3. 3.Weldon School of Biomedical EngineeringPurdue UniversityWest LafayetteUSA
  4. 4.Department of BioengineeringUniversity of Texas at DallasRichardsonUSA
  5. 5.Department of RadiologyUniversity of Texas Southwestern Medical CenterDallasUSA

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