Research progress of gene-based therapeutic angiogenesis in lower limb ischemia_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

GUI Liang ^1,2 ,  LI Yongjun ¹

1. Department of Vascular Surgery, Beijing Hospital; National Center of Gerontology; Institute of Geriatric Medicine, Chinese Academy of Medical Science and Peking Union Medical College; Beijing 100730, P. R. China;
2. Chinese Academy of Medical Sciences, Graduate School of Peking Union Medical College, Beijing 100730, P. R. China;

Corresponding author：

LI Yongjun, Email: liyongjun4679@bjhmoh.cn

Keywords：

lower limb ischemia; therapeutic angiogenesis; gene therapy; angiogenesis; gene vector

DOI：

10.7507/1007-9424.202111071

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of gene-based therapeutic angiogenesis in lower limb ischemia, so as to provide a new method for non-invasive treatment of lower limb ischemia. Method The literatures on studies of gene-based therapeutic angiogenesis in lower limb ischemia in recent years were read and reviewed. Results The incidence of peripheral arterial disease had been increasing annually. How to effectively reduce the amputation rate and mortality rate of patients with critical limb ischemia was still a clinical problem that needs to be solved urgently. A large number of basic and clinical studies had shown that gene-based therapeutic angiogenesis could effectively induce angiogenesis and collateral circulation in ischemic tissue of lower limb, leading to the significant improvements of blood perfusion in ischemic areas. Additionally, the construction of many kinds of new non-viral gene delivery vectors could also improve the safety and effectiveness of gene therapy to a certain extent. Conclusion Although promising therapeutic effect of gene-based therapeutic angiogenesis brings new ideas and strategies for the treatment of lower limb ischemia, issues still exist that have not been solved.

Citation： GUI Liang, LI Yongjun. Research progress of gene-based therapeutic angiogenesis in lower limb ischemia. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(8): 1083-1089. doi: 10.7507/1007-9424.202111071 Copy

1.	Søgaard M, Nielsen PB, Skjøth F, et al. Temporal changes in secondary prevention and cardiovascular outcomes after revascularization for peripheral arterial disease in Denmark: A nationwide cohort study. Circulation, 2021, 143(9): 907-920.
2.	Chou TH, Stacy MR. Clinical applications for radiotracer imaging of lower extremity peripheral arterial disease and critical limb ischemia. Mol Imaging Biol, 2020, 22(2): 245-255.
3.	Marsico G, Martin-Saldaña S, Pandit A. Therapeutic biomaterial approaches to alleviate chronic limb threatening ischemia. Adv Sci (Weinh), 2021, 8(7): 2003119. doi: 10.1002/advs.202003119.
4.	Gao W, Chen D, Liu G, et al. Autologous stem cell therapy for peripheral arterial disease: a systematic review and meta-analysis of randomized controlled trials. Stem Cell Res Ther, 2019, 10(1): 140. doi: 10.1186/s13287-019-1254-5.
5.	Duan J, Chen Z, Liang X, et al. Construction and application of therapeutic metal-polyphenol capsule for peripheral artery disease. Biomaterials, 2020, 255: 120199. doi: 10.1016/j.biomaterials.2020.120199.
6.	Isner JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest, 1999, 103(9): 1231-1236.
7.	Chen Z, Duan J, Diao Y, et al. ROS-responsive capsules engineered from EGCG-Zinc networks improve therapeutic angiogenesis in mouse limb ischemia. Bioact Mater, 2020, 6(1): 1-11.
8.	Marziano C, Genet G, Hirschi KK. Vascular endothelial cell specification in health and disease. Angiogenesis, 2021, 24(2): 213-236.
9.	Simons M. Angiogenesis: where do we stand now? Circulation, 2005, 111(12): 1556-1566.
10.	Monaghan RM, Page DJ, Ostergaard P, et al. The physiological and pathological functions of VEGFR3 in cardiac and lymphatic development and related diseases. Cardiovasc Res, 2021, 117(8): 1877-1890.
11.	Kitrou P, Karnabatidis D, Brountzos E, et al. Gene-based therapies in patients with critical limb ischemia. Expert Opin Biol Ther, 2017, 17(4): 449-456.
12.	Hutchings G, Kruszyna Ł, Nawrocki MJ, et al. Molecular mechanisms associated with ROS-dependent angiogenesis in lower extremity artery disease. Antioxidants (Basel), 2021, 10(5): 735. doi: 10.3390/antiox10050735.
13.	Luttun A, Carmeliet P. De novo vasculogenesis in the heart. Cardiovasc Res, 2003, 58(2): 378-389.
14.	Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science, 1997, 275(5302): 964-967.
15.	Rajagopalan S, Olin J, Deitcher S, et al. Use of a constitutively active hypoxia-inducible factor-1alpha transgene as a therapeutic strategy in no-option critical limb ischemia patients: phase Ⅰ dose-escalation experience. Circulation, 2007, 115(10): 1234-1243.
16.	Ido A, Moriuchi A, Numata M, et al. Safety and pharmacokinetics of recombinant human hepatocyte growth factor (rh-HGF) in patients with fulminant hepatitis: a phase Ⅰ / Ⅱ clinical trial, following preclinical studies to ensure safety. J Transl Med, 2011, 9: 55.
17.	Baumgartner I, Pieczek A, Manor O, et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation, 1998, 97(12): 1114-1123.
18.	Mäkinen K, Manninen H, Hedman M, et al. Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled, double-blinded phase Ⅱ study. Mol Ther, 2002, 6(1): 127-133.
19.	Rajagopalan S, Mohler ER, Lederman RJ, et al. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase Ⅱ randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation, 2003, 108(16): 1933-1938.
20.	Kusumanto YH, van Weel V, Mulder NH, et al. Treatment with intramuscular vascular endothelial growth factor gene compared with placebo for patients with diabetes mellitus and critical limb ischemia: a double-blind randomized trial. Hum Gene Ther, 2006, 17(6): 683-691.
21.	Comerota AJ, Throm RC, Miller KA, et al. Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: preliminary results of a phase Ⅰ trial. J Vasc Surg, 2002, 35(5): 930-936.
22.	Nikol S, Baumgartner I, Van Belle E, et al. Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia. Mol Ther, 2008, 16(5): 972-978.
23.	Belch J, Hiatt WR, Baumgartner I, et al. Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. Lancet, 2011, 377(9781): 1929-1937.
24.	Morishita R, Makino H, Aoki M, et al. Phase Ⅰ / Ⅱ a clinical trial of therapeutic angiogenesis using hepatocyte growth factor gene transfer to treat critical limb ischemia. Arterioscler Thromb Vasc Biol, 2011, 31(3): 713-720.
25.	Makino H, Aoki M, Hashiya N, et al. Long-term follow-up evaluation of results from clinical trial using hepatocyte growth factor gene to treat severe peripheral arterial disease. Arterioscler Thromb Vasc Biol, 2012, 32(10): 2503-2509.
26.	Powell RJ, Simons M, Mendelsohn FO, et al. Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation, 2008, 118(1): 58-65.
27.	Shigematsu H, Yasuda K, Iwai T, et al. Randomized, double-blind, placebo-controlled clinical trial of hepatocyte growth factor plasmid for critical limb ischemia. Gene Ther, 2010, 17(9): 1152-1161.
28.	Räsänen M, Sultan I, Paech J, et al. VEGF-B promotes endocardium-derived coronary vessel development and cardiac regeneration. Circulation, 2021, 143(1): 65-77.
29.	Ehrbar M, Djonov VG, Schnell C, et al. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ Res, 2004, 94(8): 1124-1132.
30.	Mac Gabhann F, Qutub AA, Annex BH, et al. Systems biology of pro-angiogenic therapies targeting the VEGF system. Wiley Interdiscip Rev Syst Biol Med, 2010, 2（6）: 694-707.
31.	Mac Gabhann F, Annex BH, Popel AS. Gene therapy from the perspective of systems biology. Curr Opin Mol Ther, 2010, 12(5): 570-577.
32.	Sanada F, Taniyama Y, Azuma J, et al. Therapeutic angiogenesis by gene therapy for critical limb ischemia: choice of biological agent. Immunol Endocr Metab Agents Med Chem, 2014, 14(1): 32-39.
33.	Sanada F, Taniyama Y, Kanbara Y, et al. Gene therapy in peripheral artery disease. Expert Opin Biol Ther, 2015, 15(3): 381-390.
34.	Taniyama Y, Morishita R, Hiraoka K, et al. Therapeutic angiogenesis induced by human hepatocyte growth factor gene in rat diabetic hind limb ischemia model: molecular mechanisms of delayed angiogenesis in diabetes. Circulation, 2001, 104(19): 2344-2350.
35.	Morishita R, Aoki M, Hashiya N, et al. Safety evaluation of clinical gene therapy using hepatocyte growth factor to treat peripheral arterial disease. Hypertension, 2004, 44(2): 203-209.
36.	Cui S, Guo L, Li X, et al. Clinical safety and preliminary efficacy of plasmid pUDK-HGF expressing human hepatocyte growth factor (HGF) in patients with critical limb ischemia. Eur J Vasc Endovasc Surg, 2015, 50(4): 494-501.
37.	Banai S, Shweiki D, Pinson A, et al. Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis. Cardiovasc Res, 1994, 28(8): 1176-1179.
38.	Gonçalves LM. Fibroblast growth factor-mediated angiogenesis for the treatment of ischemia. Lessons learned from experimental models and early human experience. Rev Port Cardiol, 1998, 17 Suppl 2: Ⅱ11-Ⅱ20.
39.	Semenza GL. Life with oxygen. Science, 2007, 318(5847): 62-64.
40.	Gui L, Chen Y, Diao Y, et al. ROS-responsive nanoparticle-mediated delivery of CYP2J2 gene for therapeutic angiogenesis in severe hindlimb ischemia. Mater Today Bio, 2021, 13: 100192. doi: 10.1016/j.mtbio.2021.100192 .
41.	Creager MA, Olin JW, Belch JJ, et al. Effect of hypoxia-inducible factor-1alpha gene therapy on walking performance in patients with intermittent claudication. Circulation, 2011, 124(16): 1765-1773.
42.	Hashem FM, Nasr M, Khairy A, et al. In vitro cytotoxicity and transfection efficiency of pDNA encoded p53 gene-loaded chitosan-sodium deoxycholate nanoparticles. Int J Nanomedicine, 2019, 14: 4123-4131.
43.	Wilhelm S, Tavares AJ, Dai Q, et al. Analysis of nanoparticle delivery to tumours. Nature Reviews Materials, 2016, 1(5): 16014. doi: 10.1038/natrevmats.2016.14.
44.	Virus used in gene therapies may pose cancer risk, dog study hints. 6 JAN 2020.https://www.science.org/content/article/virus-used-gene-therapies-may-pose-cancer-risk-dog-study-hints.
45.	Hardee CL, Arévalo-Soliz LM, Hornstein BD, et al. Advances in non-viral DNA vectors for gene therapy. Genes (Basel), 2017, 8(2): 65. doi: 10.3390/genes8020065.
46.	Jin L, Zeng X, Liu M, et al. Current progress in gene delivery technology based on chemical methods and nano-carriers. Theranostics, 2014, 4(3): 240-255.
47.	Pezzoli D, Kajaste-Rudnitski A, Chiesa R, et al. Lipid-based nanoparticles as nonviral gene delivery vectors. Methods Mol Biol, 2013, 1025: 269-279.
48.	Natsume A, Mizuno M, Ryuke Y, et al. Antitumor effect and cellular immunity activation by murine interferon-beta gene transfer against intracerebral glioma in mouse. Gene Ther, 1999, 6(9): 1626-1633.
49.	Fisher RK, Mattern-Schain SI, Best MD, et al. Improving the efficacy of liposome-mediated vascular gene therapy via lipid surface modifications. J Surg Res, 2017, 219: 136-144.
50.	Arima H, Motoyama K, Higashi T. Polyamidoamine dendrimer conjugates with cyclodextrins as novel carriers for DNA, shRNA and siRNA. Pharmaceutics, 2012, 4(1): 130-148.
51.	Fang Z, Ge X, Chen X, et al. Enhancement of sciatic nerve regeneration with dual delivery of vascular endothelial growth factor and nerve growth factor genes. J Nanobiotechnology, 2020, 18(1): 46. doi: 10.1186/s12951-020-00606-5.
52.	Chen K, Cao X, Li M, et al. A TRAIL-delivered lipoprotein-bioinspired nanovector engineering stem cell-based platform for inhibition of lung metastasis of melanoma. Theranostics, 2019, 9(10): 2984-2998.
53.	Liu X, Mo Y, Liu X, et al. Synthesis, characterisation and preliminary investigation of the haemocompatibility of polyethyleneimine-grafted carboxymethyl chitosan for gene delivery. Mater Sci Eng C Mater Biol Appl, 2016, 62: 173-182.
54.	Huo H, Gao Y, Wang Y, et al. Polyion complex micelles composed of pegylated polyasparthydrazide derivatives for siRNA delivery to the brain. J Colloid Interface Sci, 2015, 447: 8-15.
55.	Encabo-Berzosa MM, Sancho-Albero M, Sebastian V, et al. Polymer functionalized gold nanoparticles as nonviral gene delivery reagents. J Gene Med, 2017, 19(6-7). doi: 10.1002/jgm.2964.
56.	Tian A, Yang C, Zhu B, et al. Polyethylene-glycol-coated gold nanoparticles improve cardiac function after myocardial infarction in mice. Can J Physiol Pharmacol, 2018, 96(12): 1318-1327.
57.	Wu X, Wu M, Zhao JX. Recent development of silica nanoparticles as delivery vectors for cancer imaging and therapy. Nanomedicine, 2014, 10(2): 297-312.
58.	Sun L, Wang D, Chen Y, et al. Core-shell hierarchical mesostructured silica nanoparticles for gene/chemo-synergetic stepwise therapy of multidrug-resistant cancer. Biomaterials, 2017, 133: 219-228.

1. Søgaard M, Nielsen PB, Skjøth F, et al. Temporal changes in secondary prevention and cardiovascular outcomes after revascularization for peripheral arterial disease in Denmark: A nationwide cohort study. Circulation, 2021, 143(9): 907-920.
2. Chou TH, Stacy MR. Clinical applications for radiotracer imaging of lower extremity peripheral arterial disease and critical limb ischemia. Mol Imaging Biol, 2020, 22(2): 245-255.
3. Marsico G, Martin-Saldaña S, Pandit A. Therapeutic biomaterial approaches to alleviate chronic limb threatening ischemia. Adv Sci (Weinh), 2021, 8(7): 2003119. doi: 10.1002/advs.202003119.
4. Gao W, Chen D, Liu G, et al. Autologous stem cell therapy for peripheral arterial disease: a systematic review and meta-analysis of randomized controlled trials. Stem Cell Res Ther, 2019, 10(1): 140. doi: 10.1186/s13287-019-1254-5.
5. Duan J, Chen Z, Liang X, et al. Construction and application of therapeutic metal-polyphenol capsule for peripheral artery disease. Biomaterials, 2020, 255: 120199. doi: 10.1016/j.biomaterials.2020.120199.
6. Isner JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest, 1999, 103(9): 1231-1236.
7. Chen Z, Duan J, Diao Y, et al. ROS-responsive capsules engineered from EGCG-Zinc networks improve therapeutic angiogenesis in mouse limb ischemia. Bioact Mater, 2020, 6(1): 1-11.
8. Marziano C, Genet G, Hirschi KK. Vascular endothelial cell specification in health and disease. Angiogenesis, 2021, 24(2): 213-236.
9. Simons M. Angiogenesis: where do we stand now? Circulation, 2005, 111(12): 1556-1566.
10. Monaghan RM, Page DJ, Ostergaard P, et al. The physiological and pathological functions of VEGFR3 in cardiac and lymphatic development and related diseases. Cardiovasc Res, 2021, 117(8): 1877-1890.
11. Kitrou P, Karnabatidis D, Brountzos E, et al. Gene-based therapies in patients with critical limb ischemia. Expert Opin Biol Ther, 2017, 17(4): 449-456.
12. Hutchings G, Kruszyna Ł, Nawrocki MJ, et al. Molecular mechanisms associated with ROS-dependent angiogenesis in lower extremity artery disease. Antioxidants (Basel), 2021, 10(5): 735. doi: 10.3390/antiox10050735.
13. Luttun A, Carmeliet P. De novo vasculogenesis in the heart. Cardiovasc Res, 2003, 58(2): 378-389.
14. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science, 1997, 275(5302): 964-967.
15. Rajagopalan S, Olin J, Deitcher S, et al. Use of a constitutively active hypoxia-inducible factor-1alpha transgene as a therapeutic strategy in no-option critical limb ischemia patients: phase Ⅰ dose-escalation experience. Circulation, 2007, 115(10): 1234-1243.
16. Ido A, Moriuchi A, Numata M, et al. Safety and pharmacokinetics of recombinant human hepatocyte growth factor (rh-HGF) in patients with fulminant hepatitis: a phase Ⅰ / Ⅱ clinical trial, following preclinical studies to ensure safety. J Transl Med, 2011, 9: 55.
17. Baumgartner I, Pieczek A, Manor O, et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation, 1998, 97(12): 1114-1123.
18. Mäkinen K, Manninen H, Hedman M, et al. Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled, double-blinded phase Ⅱ study. Mol Ther, 2002, 6(1): 127-133.
19. Rajagopalan S, Mohler ER, Lederman RJ, et al. Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase Ⅱ randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation, 2003, 108(16): 1933-1938.
20. Kusumanto YH, van Weel V, Mulder NH, et al. Treatment with intramuscular vascular endothelial growth factor gene compared with placebo for patients with diabetes mellitus and critical limb ischemia: a double-blind randomized trial. Hum Gene Ther, 2006, 17(6): 683-691.
21. Comerota AJ, Throm RC, Miller KA, et al. Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: preliminary results of a phase Ⅰ trial. J Vasc Surg, 2002, 35(5): 930-936.
22. Nikol S, Baumgartner I, Van Belle E, et al. Therapeutic angiogenesis with intramuscular NV1FGF improves amputation-free survival in patients with critical limb ischemia. Mol Ther, 2008, 16(5): 972-978.
23. Belch J, Hiatt WR, Baumgartner I, et al. Effect of fibroblast growth factor NV1FGF on amputation and death: a randomised placebo-controlled trial of gene therapy in critical limb ischaemia. Lancet, 2011, 377(9781): 1929-1937.
24. Morishita R, Makino H, Aoki M, et al. Phase Ⅰ / Ⅱ a clinical trial of therapeutic angiogenesis using hepatocyte growth factor gene transfer to treat critical limb ischemia. Arterioscler Thromb Vasc Biol, 2011, 31(3): 713-720.
25. Makino H, Aoki M, Hashiya N, et al. Long-term follow-up evaluation of results from clinical trial using hepatocyte growth factor gene to treat severe peripheral arterial disease. Arterioscler Thromb Vasc Biol, 2012, 32(10): 2503-2509.
26. Powell RJ, Simons M, Mendelsohn FO, et al. Results of a double-blind, placebo-controlled study to assess the safety of intramuscular injection of hepatocyte growth factor plasmid to improve limb perfusion in patients with critical limb ischemia. Circulation, 2008, 118(1): 58-65.
27. Shigematsu H, Yasuda K, Iwai T, et al. Randomized, double-blind, placebo-controlled clinical trial of hepatocyte growth factor plasmid for critical limb ischemia. Gene Ther, 2010, 17(9): 1152-1161.
28. Räsänen M, Sultan I, Paech J, et al. VEGF-B promotes endocardium-derived coronary vessel development and cardiac regeneration. Circulation, 2021, 143(1): 65-77.
29. Ehrbar M, Djonov VG, Schnell C, et al. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ Res, 2004, 94(8): 1124-1132.
30. Mac Gabhann F, Qutub AA, Annex BH, et al. Systems biology of pro-angiogenic therapies targeting the VEGF system. Wiley Interdiscip Rev Syst Biol Med, 2010, 2（6）: 694-707.
31. Mac Gabhann F, Annex BH, Popel AS. Gene therapy from the perspective of systems biology. Curr Opin Mol Ther, 2010, 12(5): 570-577.
32. Sanada F, Taniyama Y, Azuma J, et al. Therapeutic angiogenesis by gene therapy for critical limb ischemia: choice of biological agent. Immunol Endocr Metab Agents Med Chem, 2014, 14(1): 32-39.
33. Sanada F, Taniyama Y, Kanbara Y, et al. Gene therapy in peripheral artery disease. Expert Opin Biol Ther, 2015, 15(3): 381-390.
34. Taniyama Y, Morishita R, Hiraoka K, et al. Therapeutic angiogenesis induced by human hepatocyte growth factor gene in rat diabetic hind limb ischemia model: molecular mechanisms of delayed angiogenesis in diabetes. Circulation, 2001, 104(19): 2344-2350.
35. Morishita R, Aoki M, Hashiya N, et al. Safety evaluation of clinical gene therapy using hepatocyte growth factor to treat peripheral arterial disease. Hypertension, 2004, 44(2): 203-209.
36. Cui S, Guo L, Li X, et al. Clinical safety and preliminary efficacy of plasmid pUDK-HGF expressing human hepatocyte growth factor (HGF) in patients with critical limb ischemia. Eur J Vasc Endovasc Surg, 2015, 50(4): 494-501.
37. Banai S, Shweiki D, Pinson A, et al. Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis. Cardiovasc Res, 1994, 28(8): 1176-1179.
38. Gonçalves LM. Fibroblast growth factor-mediated angiogenesis for the treatment of ischemia. Lessons learned from experimental models and early human experience. Rev Port Cardiol, 1998, 17 Suppl 2: Ⅱ11-Ⅱ20.
39. Semenza GL. Life with oxygen. Science, 2007, 318(5847): 62-64.
40. Gui L, Chen Y, Diao Y, et al. ROS-responsive nanoparticle-mediated delivery of CYP2J2 gene for therapeutic angiogenesis in severe hindlimb ischemia. Mater Today Bio, 2021, 13: 100192. doi: 10.1016/j.mtbio.2021.100192 .
41. Creager MA, Olin JW, Belch JJ, et al. Effect of hypoxia-inducible factor-1alpha gene therapy on walking performance in patients with intermittent claudication. Circulation, 2011, 124(16): 1765-1773.
42. Hashem FM, Nasr M, Khairy A, et al. In vitro cytotoxicity and transfection efficiency of pDNA encoded p53 gene-loaded chitosan-sodium deoxycholate nanoparticles. Int J Nanomedicine, 2019, 14: 4123-4131.
43. Wilhelm S, Tavares AJ, Dai Q, et al. Analysis of nanoparticle delivery to tumours. Nature Reviews Materials, 2016, 1(5): 16014. doi: 10.1038/natrevmats.2016.14.
44. Virus used in gene therapies may pose cancer risk, dog study hints. 6 JAN 2020.https://www.science.org/content/article/virus-used-gene-therapies-may-pose-cancer-risk-dog-study-hints.
45. Hardee CL, Arévalo-Soliz LM, Hornstein BD, et al. Advances in non-viral DNA vectors for gene therapy. Genes (Basel), 2017, 8(2): 65. doi: 10.3390/genes8020065.
46. Jin L, Zeng X, Liu M, et al. Current progress in gene delivery technology based on chemical methods and nano-carriers. Theranostics, 2014, 4(3): 240-255.
47. Pezzoli D, Kajaste-Rudnitski A, Chiesa R, et al. Lipid-based nanoparticles as nonviral gene delivery vectors. Methods Mol Biol, 2013, 1025: 269-279.
48. Natsume A, Mizuno M, Ryuke Y, et al. Antitumor effect and cellular immunity activation by murine interferon-beta gene transfer against intracerebral glioma in mouse. Gene Ther, 1999, 6(9): 1626-1633.
49. Fisher RK, Mattern-Schain SI, Best MD, et al. Improving the efficacy of liposome-mediated vascular gene therapy via lipid surface modifications. J Surg Res, 2017, 219: 136-144.
50. Arima H, Motoyama K, Higashi T. Polyamidoamine dendrimer conjugates with cyclodextrins as novel carriers for DNA, shRNA and siRNA. Pharmaceutics, 2012, 4(1): 130-148.
51. Fang Z, Ge X, Chen X, et al. Enhancement of sciatic nerve regeneration with dual delivery of vascular endothelial growth factor and nerve growth factor genes. J Nanobiotechnology, 2020, 18(1): 46. doi: 10.1186/s12951-020-00606-5.
52. Chen K, Cao X, Li M, et al. A TRAIL-delivered lipoprotein-bioinspired nanovector engineering stem cell-based platform for inhibition of lung metastasis of melanoma. Theranostics, 2019, 9(10): 2984-2998.
53. Liu X, Mo Y, Liu X, et al. Synthesis, characterisation and preliminary investigation of the haemocompatibility of polyethyleneimine-grafted carboxymethyl chitosan for gene delivery. Mater Sci Eng C Mater Biol Appl, 2016, 62: 173-182.
54. Huo H, Gao Y, Wang Y, et al. Polyion complex micelles composed of pegylated polyasparthydrazide derivatives for siRNA delivery to the brain. J Colloid Interface Sci, 2015, 447: 8-15.
55. Encabo-Berzosa MM, Sancho-Albero M, Sebastian V, et al. Polymer functionalized gold nanoparticles as nonviral gene delivery reagents. J Gene Med, 2017, 19(6-7). doi: 10.1002/jgm.2964.
56. Tian A, Yang C, Zhu B, et al. Polyethylene-glycol-coated gold nanoparticles improve cardiac function after myocardial infarction in mice. Can J Physiol Pharmacol, 2018, 96(12): 1318-1327.
57. Wu X, Wu M, Zhao JX. Recent development of silica nanoparticles as delivery vectors for cancer imaging and therapy. Nanomedicine, 2014, 10(2): 297-312.
58. Sun L, Wang D, Chen Y, et al. Core-shell hierarchical mesostructured silica nanoparticles for gene/chemo-synergetic stepwise therapy of multidrug-resistant cancer. Biomaterials, 2017, 133: 219-228.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of gene-based therapeutic angiogenesis in lower limb ischemia

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