Advances in Clinical and Experimental Medicine

Title abbreviation: Adv Clin Exp Med
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Advances in Clinical and Experimental Medicine

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doi: 10.17219/acem/134115

Publication type: original article

Language: English

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Low-intensity pulsed ultrasound enhances angiogenesis in rabbit capsule tissue that acts as a novel vascular bed in vivo

Mingming Yu1,2,A,B,D, Yu Bian2,C, Lin Wang1,2,B, Fang Chen1,2,E,F

1 Department of Urology, Shanghai Children’s Hospital, Shanghai Jiao Tong University, China

2 Department of Urology, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, China

Abstract

Background. In vivo prevascularization followed by pedicled transfer has emerged as a promising strategy for tissue engineering in recent years. We recently demonstrated that capsule tissue could serve as a novel axial in vivo vascular bed, although its high-density microvessels could only be maintained for about a week.
Objectives. In this present study, we aimed to demonstrate whether low-intensity pulsed ultrasound (LIPUS) promotes angiogenesis in capsule tissue.
Material and Methods. After successful induction of capsule tissue using a skin expander, 24 rabbits were randomly divided into the LIPUS group and the control group. The LIPUS group received LIPUS treatment 3 times per week. After 2 and 4 weeks of treatment, angiogenesis of the capsule tissue was assessed using in vivo and in vitro methods, including contrast-enhanced ultrasound (CEUS), photoacoustic imaging (PAI), photoacoustic microscope (PAM), and CD31 immunohistochemistry.
Results. In vivo assessments (CEUS, PAI and PAM) showed that tissue perfusion, hemoglobin content and vascular density were all significantly higher in the LIPUS group, which was consistent with CD31 immunohistochemistry. The LIPUS also promoted protein and mRNA expression of vascular endothelial growth factor α (VEGFα) and basic fibroblast growth factor (bFGF) in capsule tissue. Furthermore, cell experiments showed that LIPUS enhanced tube formation of human microvascular endothelial cells (HMECs) and promoted secretion of VEGFα and bFGF.
Conclusion. The LIPUS treatment promoted angiogenesis of the capsule tissue by stimulating release of angiogenic factors such as VEGFα and bFGF from endothelial cells, making the capsule tissue more potent and sustained when acting as in vivo vascular bed.

Key words

low-intensity pulsed ultrasound, capsule tissue, angiogenesis, vascular bed, tissue engineering

References (29)

  1. Kant RJ, Coulombe KLK. Integrated approaches to spatiotemporally directing angiogenesis in host and engineered tissues. Acta Biomater. 2018;69:42–62. doi:10.1016/j.actbio.2018.01.017
  2. Epple C, Haumer A, Ismail T, et al. Prefabrication of a large pedicled bone graft by engineering the germ for de novo vascularization and osteoinduction. Biomaterials. 2019;192:118–127. doi:10.1016/j.biomaterials.2018.11.008
  3. Rnjak-Kovacina J, Gerrand YW, Wray LS, et al. Vascular pedicle and microchannels: Simple methods toward effective in vivo vascularization of 3D scaffolds. Adv Healthc Mater. 2019;8(24):e1901106. doi:10.1002/adhm.201901106
  4. Bengtson BP, Ringler SL, George ER, DeHaan MR, Mills KA. Capsular tissue: A new local flap. Plast Reconstr Surg. 1993;91(6):1073–1079. doi:10.1097/00006534-199305000-00016
  5. Schoeller T, Lille S, Stenzl A, et al. Bladder reconstruction using a prevascularized capsular tissue seeded with urothelial cells. J Urol. 2001;165(3):980–985. PMID:11176526
  6. Geelhoed WJ, van der Bogt KEA, Rothuizen TC, et al. A novel method for engineering autologous non-thrombogenic in situ tissue-engineered blood vessels for arteriovenous grafting. Biomaterials. 2020;229:119577. doi:10.1016/j.biomaterials.2019.119577
  7. DeGeorge Br Jr, Campbell CA. Techniques to refine the upper outer breast aesthetic subunit in alloplastic breast reconstruction: The lateral capsular flap. Plast Surg (Oakv). 2016;24(2):83–88. doi:10.4172/plastic-surgery.1000966
  8. Josiassen M, Kudibal MT, Gramkow C, Trojahn Kølle SF. Closure of thoracic wall defect using breast implant capsule tissue as a rotation flap: A case report. Case Reports Plast Surg Hand Surg. 2018;5(1):39–40. doi:10.1080/23320885.2018.1476150
  9. Jia Z, Guo H, Xie H, et al. Construction of pedicled smooth muscle tissues by combining the capsule tissue and cell sheet engineering. Cell Transplant. 2019;28(3):328–342. doi:10.1177/0963689718821682
  10. Guo HL, Peng XF, Bao XQ, et al. Bladder reconstruction using autologous smooth muscle cell sheets grafted on a pre-vascularized capsule. Theranostics. 2020;10(23):10378–10393. doi:10.7150/thno.47006
  11. Guo HL, Wang L, Jia ZM, et al. Tissue expander capsule as an induced vascular bed to prefabricate an axial vascularized buccal mucosa-lined flap for tubularized posterior urethral reconstruction: Preliminary results in an animal model. Asian J Androl. 2020;22(5):459–464. doi:10.4103/aja.aja_133_19
  12. Guo HL, Jia ZM, Wang L, et al. Tubularized urethral reconstruction using a prevascularized capsular tissue prelaminated with buccal mucosa graft in a rabbit model. Asian J Androl. 2019;21(4):381–386. doi:10.4103/aja.aja_43_19
  13. Kang PL, Huang HH, Chen T, Ju KC, Kuo SM. Angiogenesis-promoting effect of LIPUS on hADSCs and HUVECs cultured on collagen/hyaluronan scaffolds. Mater Sci Eng C Mater Biol Appl. 2019;102:22–33. doi:10.1016/j.msec.2019.04.045
  14. Ogata T, Ito K, Shindo T, et al. Low-intensity pulsed ultrasound enhances angiogenesis and ameliorates contractile dysfunction of pressure-overloaded heart in mice. PLoS One. 2017;12(9):e0185555. doi:10.1371/journal.pone.0185555
  15. Kamatsuki Y, Aoyama E, Furumatsu T, et al. Possible reparative effect of low-intensity pulsed ultrasound (LIPUS) on injured meniscus. J Cell Commun Signal. 2019;13(2):193–207. doi:10.1007/s12079-018-0496-9
  16. Hanawa K, Ito K, Aizawa K, et al. Low-intensity pulsed ultrasound induces angiogenesis and ameliorates left ventricular dysfunction in a porcine model of chronic myocardial ischemia. PLoS One. 2014;9(8):e104863. doi:10.1371/journal.pone.0104863
  17. Su Z, Xu T, Wang Y, et al. Low intensity pulsed ultrasound promotes apoptosis and inhibits angiogenesis via p38 signaling mediated endoplasmic reticulum stress in human endothelial cells. Mol Med Rep. 2019;19(6):4645–4654. doi:10.3892/mmr.2019.10136
  18. Gholobova D, Terrie L, Mackova K, et al. Functional evaluation of prevascularization in one-stage versus two-stage tissue engineering approach of human bio-artificial muscle. Biofabrication. 2020;12(3):035021. doi:10.1088/1758-5090/ab8f36
  19. Adamowicz J, Pokrywczynska M, Van Breda SV, Kloskowski T, Drewa T. Concise review: Tissue engineering of urinary bladder. We still have a long way to go? Stem Cells Transl Med. 2017;6(11):2033–2043. doi:10.1002/sctm.17-0101
  20. Utzinger U, Baggett B, Weiss JA, Hoying JB, Edgar LT. Large-scale time series microscopy of neovessel growth during angiogenesis. Angiogenesis. 2015;18(3):219–232. doi:10.1007/s10456-015-9461-x
  21. Kastellorizios M, Tipnis N, Burgess DJ. Foreign body reaction to subcutaneous implants. Adv Exp Med Biol. 2015;865:93–108. doi:10.1007/978-3-319-18603-0_6
  22. Klopfleisch R, Jung F. The pathology of the foreign body reaction against biomaterials. J Biomed Mater Res A. 2017;105(3):927–940. doi:10.1002/jbm.a.35958
  23. Huang JJ, Shi YQ, Li RL, et al. Angiogenesis effect of therapeutic ultrasound on HUVECs through activation of the PI3K-Akt-eNOS signal pathway. Am J Transl Res. 2015;7(6):1106–1115. PMID:26279754
  24. Xu XM, Xu TM, Wei YB, et al. Low-intensity pulsed ultrasound treatment accelerates angiogenesis by activating YAP/TAZ in human umbilical vein endothelial cells. Ultrasound Med Biol. 2018;44(12):2655–2661. doi:10.1016/j.ultrasmedbio.2018.07.007
  25. Costa V, Carina V, Conigliaro A, et al. miR-31-5p Is a LIPUS-mechanosensitive microRNA that targets HIF-1α signaling and cytoskeletal proteins. Int J Mol Sci. 2019;20(7):1569. doi:10.3390/ijms20071569
  26. Hassan MA, Campbell P, Kondo T. The role of Ca(2+) in ultrasound-elicited bioeffects: Progress, perspectives and prospects. Drug Discov Today. 2010;15(21–22):892–906. doi:10.1016/j.drudis.2010.08.005
  27. Lau C, Rivas M, Dinalo J, King K, Duddalwar V. Scoping review of targeted ultrasound contrast agents in the detection of angiogenesis. J Ultrasound Med. 2020;39(1):19–28. doi:10.1002/jum.15072
  28. Ogunlade O, Ho JOY, Kalber TL, et al. Monitoring neovascularization and integration of decellularized human scaffolds using photoacoustic imaging. Photoacoustics. 2019;13:76–84. doi:10.1016/j.pacs.2019.01.001
  29. Yang F, Wang Z, Zhang W, et al. Wide-field monitoring and real-time local recording of microvascular networks on small animals with a dual-raster-scanned photoacoustic microscope. J Biophotonics. 2020;13(6):e202000022. doi:10.1002/jbio.202000022
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