Overcoming big bottlenecks in vascular regeneration – Communications Biology

  • Cardiovascular Diseases. World Health Organization, accessed 12/03/2023. https://www.who.int/health-topics/cardiovascular-diseases (2023).

  • Mathur, A., Mohan, V., Ameta, D., Gaurav, B. & Haranahalli, P. Aortic aneurysm. J. Transl. Int. Med. 4, 35–41 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Phillippi, J. A. On vasa vasorum: A history of advances in understanding the vessels of vessels. Sci. Adv. 8, eabl6364 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Salmasi, M. Y. et al. Regional variation in biomechanical properties of ascending thoracic aortic aneurysms. Eur. J. Cardiothorac. Surg. 62, ezac392 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, C. et al. Aortic stress activates an Adaptive Program in Thoracic Aortic Smooth Muscle Cells That Maintains Aortic Strength and Protects Against Aneurysm and Dissection in Mice. Arterioscler Thromb. Vasc. Biol. 43, 234–252 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Milutinovic, A., Zivin, M. & Zorc-Pleskovic, R. Differences between inflammatory cells infiltrated into tunica intima, media, and adventitia of ascending aortic aneurysms within diabetic and hypertensive patients. Biomol. Biomed. 23, 596–604 (2023).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Prall, A. K. et al. 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).

    Article 
    PubMed 

    Google Scholar
     

  • Baxter, B. T. et al. Effect of Doxycycline on Aneurysm Growth Among Patients With Small Infrarenal Abdominal Aortic Aneurysms: A Randomized Clinical Trial. JAMA 323, 2029–2038, (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Isenburg, J. C., Simionescu, D. T., Starcher, B. C. & Vyavahare, N. R. Elastin stabilization for treatment of abdominal aortic aneurysms. Circulation 115, 1729–1737 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dhital, S. & Vyavahare, N. R. Nanoparticle-based targeted delivery of pentagalloyl glucose reverses elastase-induced abdominal aortic aneurysm and restores aorta to the healthy state in mice. PLoS One 15, e0227165 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Simionescu, D. et al. Chemical stabilization of the extracellular matrix attenuates growth of experimentally induced abdominal aorta aneurysms in a large animal model. JVS Vasc. Sci. 1, 69–80 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kloster, B. O., Lund, L. & Lindholt, J. S. Inhibition of early AAA formation by aortic intraluminal pentagalloyl glucose (PGG) infusion in a novel porcine AAA model. Ann. Med Surg. (Lond.) 7, 65–70 (2016).

    Article 
    PubMed 

    Google Scholar
     

  • Nosoudi, N. et al. Prevention of abdominal aortic aneurysm progression by targeted inhibition of matrix metalloproteinase activity with batimastat-loaded nanoparticles. Circ. Res. 117, e80–e89 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sinha, A. et al. Nanoparticle targeting to diseased vasculature for imaging and therapy. Nanomedicine 10, 1003–1012 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Cheng, S. W. K. et al. A pilot study to evaluate a novel localized treatment to stabilize small- to medium-sized infrarenal abdominal aortic aneurysms. J. Vasc. Surg. 78, 929–935.e921 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • Blose, K. J. et al. Periadventitial adipose-derived stem cell treatment halts elastase-induced abdominal aortic aneurysm progression. Regen. Med. 9, 733–741 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sharma, A. K. et al. Experimental abdominal aortic aneurysm formation is mediated by IL-17 and attenuated by mesenchymal stem cell treatment. Circulation 126, S38–S45 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yamawaki-Ogata, A., Oshima, H., Usui, A. & Narita, Y. Bone marrow-derived mesenchymal stromal cells regress aortic aneurysm via the NF-kB, Smad3 and Akt signaling pathways. Cytotherapy 19, 1167–1175 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Parvizi, M., Petersen, A. H., van Spreuwel-Goossens, C., Kluijtmans, S. & Harmsen, M. C. Perivascular scaffolds loaded with adipose tissue-derived stromal cells attenuate development and progression of abdominal aortic aneurysm in rats. J. Biomed. Mater. Res A 106, 2494–2506 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Xie, J. et al. Human Adipose-Derived Stem Cells Suppress Elastase-Induced Murine Abdominal Aortic Inflammation and Aneurysm Expansion Through Paracrine Factors. Cell Transpl. 26, 173–189 (2017).

    Article 

    Google Scholar
     

  • Mulorz, J. et al. peri-Adventitial delivery of smooth muscle cells in porous collagen scaffolds for treatment of experimental abdominal aortic aneurysm. Biomater. Sci. 9, 6903–6914 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Morrison, J. J. et al. Clinical implementation of the Humacyte human acellular vessel: Implications for military and civilian trauma care. J. Trauma Acute Care Surg. 87, S44–S47 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Tsao, C. W. et al. Heart Disease and Stroke Statistics-2022 Update: A Report From the American Heart Association. Circulation 145, e153–e639 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Adams, H. P. Jr. et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 24, 35–41 (1993).

    Article 
    PubMed 

    Google Scholar
     

  • Tian, B. et al. Clinical and Imaging Indicators of Hemorrhagic Transformation in Acute Ischemic Stroke After Endovascular Thrombectomy. Stroke 53, 1674–1681 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu-Ambrose, T. et al. Effect of Exercise Training or Complex Mental and Social Activities on Cognitive Function in Adults With Chronic Stroke: A Randomized Clinical Trial. JAMA Netw. Open 5, e2236510 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kim, H. Y. et al. Mesenchymal stem cell-derived magnetic extracellular nanovesicles for targeting and treatment of ischemic stroke. Biomaterials 243, 119942 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Guo, L. et al. Enhanced pericyte-endothelial interactions through NO-boosted extracellular vesicles drive revascularization in a mouse model of ischemic injury. Nat. Commun. 14, 7334 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu, X., Geng, X., Shi, Y., Liang, J. & Zhao, L. Biomimetic oxygen-boosted hybrid membrane nanovesicles as the treatment strategy for ischemic stroke with the concept of the neurovascular unit. Biomater. Adv. 148, 213379 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ghuman, H. et al. Biodegradation of ECM hydrogel promotes endogenous brain tissue restoration in a rat model of stroke. Acta Biomater. 80, 66–84 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wu, Y. et al. Implantation of Brain-Derived Extracellular Matrix Enhances Neurological Recovery after Traumatic Brain Injury. Cell Transpl. 26, 1224–1234 (2017).

    Article 

    Google Scholar
     

  • Ghuman, H. et al. Long-term retention of ECM hydrogel after implantation into a sub-acute stroke cavity reduces lesion volume. Acta Biomater. 63, 50–63 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, H. et al. Machine Learning Approach to Identify Stroke Within 4.5 h. Stroke 51, 860–866 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Hadamitzky, C. et al. Aligned nanofibrillar collagen scaffolds – Guiding lymphangiogenesis for treatment of acquired lymphedema. Biomaterials 102, 259–267 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chung, T. K., Gueldner, P. H., Aloziem, O. U., Liang, N. L. & Vorp, D. A. An artificial intelligence based abdominal aortic aneurysm prognosis classifier to predict patient outcomes. Sci. Rep. 14, 3390 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Inampudi, C., Akintoye, E., Ando, T. & Briasoulis, A. Angiogenesis in peripheral arterial disease. Curr. Opin. Pharm. 39, 60–67 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Scully, R. E., Arnaoutakis, D. J., DeBord Smith, A., Semel, M. & Nguyen, L. L. Estimated annual health care expenditures in individuals with peripheral arterial disease. J. Vasc. Surg. 67, 558–567 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Brevetti, G., Giugliano, G., Brevetti, L. & Hiatt, W. R. Inflammation in peripheral artery disease. Circulation 122, 1862–1875 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • Murabito, J. M. et al. Cross-sectional relations of multiple inflammatory biomarkers to peripheral arterial disease: The Framingham Offspring Study. Atherosclerosis 203, 509–514 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Aday, A. W. & Everett, B. M. Dyslipidemia Profiles in Patients with Peripheral Artery Disease. Curr. Cardiol. Rep. 21, 42 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scheller, J., Chalaris, A., Schmidt-Arras, D. & Rose-John, S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys. Acta 1813, 878–888 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wolf, J., Rose-John, S. & Garbers, C. Interleukin-6 and its receptors: a highly regulated and dynamic system. Cytokine 70, 11–20 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ley, K. The role of selectins in inflammation and disease. Trends Mol. Med 9, 263–268 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Signorelli, S. S. et al. Plasma Levels of Inflammatory Biomarkers in Peripheral Arterial Disease: Results of a Cohort Study. Angiology 67, 870–874 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Szade, A., Grochot-Przeczek, A., Florczyk, U., Jozkowicz, A. & Dulak, J. Cellular and molecular mechanisms of inflammation-induced angiogenesis. IUBMB Life 67, 145–159 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Eilken, H. M. & Adams, R. H. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22, 617–625 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yang, G., Mahadik, B., Choi, J. Y. & Fisher, J. P. Vascularization in tissue engineering: fundamentals and state-of-art. Prog. Biomed. Eng. (Bristol) 2, 012002 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Li, S., Sengupta, D. & Chien, S. Vascular tissue engineering: from in vitro to in situ. Wiley Interdiscip. Rev. Syst. Biol. Med 6, 61–76 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Generali, M. et al. Autologous endothelialized small-caliber vascular grafts engineered from blood-derived induced pluripotent stem cells. Acta Biomater. 97, 333–343 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Aitsebaomo, J. et al. Recombinant human interleukin-11 treatment enhances collateral vessel growth after femoral artery ligation. Arterioscler Thromb. Vasc. Biol. 31, 306–312 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, L. et al. The roles of interleukins in perfusion recovery after peripheral arterial disease. Biosci. Rep. 38, BSR20171455 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Simons, M., Gordon, E. & Claesson-Welsh, L. Mechanisms and regulation of endothelial VEGF receptor signalling. Nat. Rev. Mol. Cell Biol. 17, 611–625 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cooke, J. P. & Meng, S. Vascular Regeneration in Peripheral Artery Disease. Arterioscler Thromb. Vasc. Biol. 40, 1627–1634 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fiedler, U. & Augustin, H. G. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 27, 552–558 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Levin, M. G. et al. A Missense Variant in the IL-6 Receptor and Protection From Peripheral Artery Disease. Circ. Res 129, 968–970 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kang, S. & Kishimoto, T. Interplay between interleukin-6 signaling and the vascular endothelium in cytokine storms. Exp. Mol. Med 53, 1116–1123 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gopinathan, G. et al. Interleukin-6 Stimulates Defective Angiogenesis. Cancer Res. 75, 3098–3107 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zbinden, J. C. et al. Effects of Braiding Parameters on Tissue Engineered Vascular Graft Development. Adv. Health. Mater. 9, e2001093 (2020).

    Article 

    Google Scholar
     

  • Corradetti, B. et al. Immune tuning scaffold for the local induction of a pro-regenerative environment. Sci. Rep. 7, 17030 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, J. B. et al. Microchannel network hydrogel induced ischemic blood perfusion connection. Nat. Commun. 11, 615 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deveza, L. et al. Polymer-DNA Nanoparticle-Induced CXCR4 Overexpression Improves Stem Cell Engraftment and Tissue Regeneration in a Mouse Hindlimb Ischemia Model. Theranostics 6, 1176–1189 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khanna, A., Oropeza, B. P. & Huang, N. F. Engineering Spatiotemporal Control in Vascularized Tissues. Bioeng. (Basel) 9, 555 (2022).

    CAS 

    Google Scholar
     

  • Khanna, A., Zamani, M. & Huang, N. F. Extracellular Matrix-Based Biomaterials for Cardiovascular Tissue Engineering. J. Cardiovasc Dev. Dis. 8, 137 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mirdamadi, E., Tashman, J. W., Shiwarski, D. J., Palchesko, R. N. & Feinberg, A. W. FRESH 3D Bioprinting a Full-Size Model of the Human Heart. ACS Biomater. Sci. Eng. 6, 6453–6459 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hinton, T. J. et al. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci. Adv. 1, e1500758 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, V. K. et al. Creating perfused functional vascular channels using 3D bio-printing technology. Biomaterials 35, 8092–8102 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pias, S. C. Pathways of Oxygen Diffusion in Cells and Tissues : Hydrophobic Channeling via Networked Lipids. Adv. Exp. Med Biol. 1232, 183–190 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Blaeser, A. et al. Controlling Shear Stress in 3D Bioprinting is a Key Factor to Balance Printing Resolution and Stem Cell Integrity. Adv. Health. Mater. 5, 326–333 (2016).

    Article 
    CAS 

    Google Scholar
     

  • Cooke, M. E. & Rosenzweig, D. H. The rheology of direct and suspended extrusion bioprinting. APL Bioeng. 5, 011502 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nesmith, J. E., Chappell, J. C., Cluceru, J. G. & Bautch, V. L. Blood vessel anastomosis is spatially regulated by Flt1 during angiogenesis. Development 144, 889–896 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hafa, L. et al. Light Sheet-based Laser Patterning Bioprinting Produces Long-term Viable Full-thickness Skin Constructs. Adv. Mater. 36, e2306258 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • Kawata, S., Sun, H. B., Tanaka, T. & Takada, K. Finer features for functional microdevices. Nature 412, 697–698 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Urciuolo, A. et al. Intravital three-dimensional bioprinting. Nat. Biomed. Eng. 4, 901–915 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar