Skip to main content

Advertisement

SpringerLink
Log in

Biological aspects in controlling angiogenesis: current progress

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

All living beings continue their life by receiving energy and by excreting waste products. In animals, the arteries are the pathways of these transfers to the cells. Angiogenesis, the formation of the arteries by the development of pre-existed parental blood vessels, is a phenomenon that occurs naturally during puberty due to certain physiological processes such as menstruation, wound healing, or the adaptation of athletes’ bodies during exercise. Nonetheless, the same life-giving process also occurs frequently in some patients and, conversely, occurs slowly in some physiological problems, such as cancer and diabetes, so inhibiting angiogenesis has been considered to be one of the important strategies to fight these diseases. Accordingly, in tissue engineering and regenerative medicine, the highly controlled process of angiogenesis is very important in tissue repairing. Excessive angiogenesis can promote tumor progression and lack of enough angiogensis can hinder tissue repair. Thereby, both excessive and deficient angiogenesis can be problematic, this review article introduces and describes the types of factors involved in controlling angiogenesis. Considering all of the existing strategies, we will try to lay out the latest knowledge that deals with stimulating/inhibiting the angiogenesis. At the end of the article, owing to the early-reviewed mechanical aspects that overshadow angiogenesis, the strategies of angiogenesis in tissue engineering will be discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of data and materials

All data generated or analyzed during this study are included in this published article.

References

  1. Folkman J (2006) Angiogenesis. J Annu Rev Med 57:1–18

    CAS  Google Scholar 

  2. Senger DR, Davis GE (2011) Angiogenesis. Cold Spring Harb Perspect Biol 3(8):a005090

    PubMed  PubMed Central  Google Scholar 

  3. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285(21):1182–1186

    CAS  PubMed  Google Scholar 

  4. Conway EM, Collen D, Carmeliet P (2001) Molecular mechanisms of blood vessel growth. Cardiovasc Res 49(3):507–521

    CAS  PubMed  Google Scholar 

  5. Ucuzian AA et al (2010) Molecular mediators of angiogenesis. J Burn Care 31(1):158–175

    Google Scholar 

  6. Nyberg P, Xie L, Kalluri R (2005) Endogenous inhibitors of angiogenesis. Can Res 65(10):3967–3979

    CAS  Google Scholar 

  7. Martínez A (2006) A new family of angiogenic factors. Cancer Lett 236(2):157–163

    PubMed  Google Scholar 

  8. Ribatti D, Crivellato E (2012) “Sprouting angiogenesis”, a reappraisal. Dev Biol 372(2):157–165

    CAS  PubMed  Google Scholar 

  9. Cai W, Schaper W (2008) Mechanisms of arteriogenesis. Acta Biochim Biophys Sin 40(8):681–692

    CAS  PubMed  Google Scholar 

  10. Krock BL et al (2011) Hypoxia-induced angiogenesis: good and evil. Genes 2(12):1117–1133

    Google Scholar 

  11. Olsson A-K et al (2006) VEGF receptor signalling? In control of vascular function. Nat Rev Mol Cell Biol 7(5):359–371

    CAS  PubMed  Google Scholar 

  12. Stepien HM et al (2002) Angiogenesis of endocrine gland tumours-new molecular targets in diagnostics and therapy. Eur J Endocrinol 146(2):143–152

    CAS  PubMed  Google Scholar 

  13. Trikha M et al (2002) Multiple roles for platelet GPIIb/IIIa and αvβ3 integrins in tumor growth, angiogenesis, and metastasis. Can Res 62(10):2824–2833

    CAS  Google Scholar 

  14. Salvucci O, Tosato G (2012) Essential roles of EphB receptors and EphrinB ligands in endothelial cell function and angiogenesis. Adv Cancer Res 114:21–57

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Folkman J (2006) Angiogenesis. Annu Rev Med 57:1–18

    CAS  PubMed  Google Scholar 

  16. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473(7347):298–307

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Kerbel RS (2008) Tumor angiogenesis. N Engl J Med 358(19):2039–2049

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Shikatani EA et al (2012) Inhibition of proliferation, migration and proteolysis contribute to corticosterone-mediated inhibition of angiogenesis. PLoS One 7:e46625

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Pasquet M et al (2010) Hospicells (ascites-derived stromal cells) promote tumorigenicity and angiogenesis. Int J Cancer 126(9):2090–2101

    CAS  PubMed  Google Scholar 

  20. Dudley AC, Cloer EW, Melero-Martin JM (2012) The role of bone marrow-derived progenitor cells in tumor growth and angiogenesis. Stem cells and cancer stem cells, vol 8. Springer, pp 45–54

    Google Scholar 

  21. Sica A et al (2006) Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 42(6):717–727

    CAS  PubMed  Google Scholar 

  22. Harrell CR et al (2018) Molecular mechanisms underlying therapeutic potential of pericytes. J Biomed Sci 25(1):1–12

    Google Scholar 

  23. Tilton RG, Kilo C, Williamson JR (1979) Pericyte-endothelial relationships in cardiac and skeletal muscle capillaries. Microvasc Res 18(3):325–335

    CAS  PubMed  Google Scholar 

  24. Shepro D, Morel NM (1993) Pericyte physiology. FASEB J 7(11):1031–1038

    CAS  PubMed  Google Scholar 

  25. Gaengel K et al (2009) Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 29(5):630–638

    CAS  PubMed  Google Scholar 

  26. Lee S et al (2010) Pericyte actomyosin-mediated contraction at the cell–material interface can modulate the microvascular niche. J Phys Condens Matter 22(19):194115

    PubMed  Google Scholar 

  27. Chen CW et al (2013) Human pericytes for ischemic heart repair. Stem Cells 31(2):305–316

    CAS  PubMed  Google Scholar 

  28. Proebstl D et al (2012) Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. J Exp Med 209(6):1219–1234

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Zanotelli MR, Reinhart-King CA (2018) Mechanical forces in tumor angiogenesis. Adv Exp Med Biol 1092:91–112. https://doi.org/10.1007/978-3-319-95294-9_6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Underwood CJ et al (2014) Cell-generated traction forces and the resulting matrix deformation modulate microvascular alignment and growth during angiogenesis. Am J Physiol Heart Circ Physiol 307(2):H152–H164

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Chicurel ME, Chen CS, Ingber DE (1998) Cellular control lies in the balance of forces. Curr Opin Cell Biol 10(2):232–239

    CAS  PubMed  Google Scholar 

  32. Galbraith CG, Sheetz MP (1998) Forces on adhesive contacts affect cell function. Curr Opin Cell Biol 10(5):566–571

    CAS  PubMed  Google Scholar 

  33. Sieminski A, Hebbel R, Gooch K (2004) The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp Cell Res 297(2):574–584

    CAS  PubMed  Google Scholar 

  34. Kuzuya M et al (1996) Inhibition of endothelial cell differentiation on a glycosylated reconstituted basement membrane complex. Exp Cell Res 226(2):336–345

    CAS  PubMed  Google Scholar 

  35. Deroanne CF, Lapiere CM, Nusgens BV (2001) In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovasc Res 49(3):647–658

    CAS  PubMed  Google Scholar 

  36. Vernon RB et al (1995) Organized type I collagen influences endothelial patterns during “spontaneous angiogenesis in vitro”: planar cultures as models of vascular development. In Vitro Cell Dev Biol Anim 31(2):120–131

    CAS  PubMed  Google Scholar 

  37. Ausprunk DH, Folkman J (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 14(1):53–65

    CAS  PubMed  Google Scholar 

  38. Shiu Y-T et al (2005) The role of mechanical stresses in angiogenesis. Crit Rev Biomed Eng 33(5):431–510

    PubMed  Google Scholar 

  39. Vernon RB et al (1992) Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. Lab Investig 66(5):536–547

    CAS  PubMed  Google Scholar 

  40. Vernon RB, Sage EH (1995) Between molecules and morphology. Extracellular matrix and creation of vascular form. Am J Pathol 147(4):873

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75(3):519–560

    CAS  PubMed  Google Scholar 

  42. Krishnan L et al (2003) Effects of angiogenesis on the material properties of the extracellular matrix: correlation with gene expression. In: Proceedings of the ASME summer bioengineering conference

  43. Clark ER (1918) Studies on the growth of blood-vessels in the tail of the frog larva—by observation and experiment on the living animal. Am J Anat 23(1):37–88

    Google Scholar 

  44. Rivilis I et al (2002) Differential involvement of MMP-2 and VEGF during muscle stretch-versus shear stress-induced angiogenesis. Am J Physiol Heart Circ Physiol 283(4):H1430–H1438

    CAS  PubMed  Google Scholar 

  45. Van Gieson EJ, Skalak TC (2001) Chronic vasodilation induces matrix metalloproteinase 9 (MMP-9) expression during microvascular remodeling in rat skeletal muscle. Microcirculation 8(1):25–31

    PubMed  Google Scholar 

  46. Egginton S et al (2001) Unorthodox angiogenesis in skeletal muscle. Cardiovasc Res 49(3):634–646

    CAS  PubMed  Google Scholar 

  47. Egginton S et al (1998) Capillary growth in relation to blood flow and performance in overloaded rat skeletal muscle. J Appl Physiol 85(6):2025–2032

    CAS  PubMed  Google Scholar 

  48. Bamias A, Dimopoulos MA (2003) Angiogenesis in human cancer: implications in cancer therapy. Eur J Intern Med 14(8):459–469

    CAS  PubMed  Google Scholar 

  49. Gupta MK, Qin R-Y (2003) Mechanism and its regulation of tumor-induced angiogenesis. World J Gastroenterol WJG 9(6):1144

    CAS  PubMed  Google Scholar 

  50. Hertig AT (1935) Angiogenesis in the early human chorion and in the primary placenta of the macaque monkey. Control Embryol 146:37–82

    Google Scholar 

  51. Martin P (1997) Wound healing–aiming for perfect skin regeneration. Science 276(5309):75–81

    CAS  PubMed  Google Scholar 

  52. Clark RA (1988) Wound repair. The molecular and cellular biology of wound repair. Springer, New York, pp 3–50

    Google Scholar 

  53. Albert S (2002) Cost-effective management of recalcitrant diabetic foot ulcers. Clin Podiatr Med 19(4):483–491

    Google Scholar 

  54. Kanitakis J (2002) Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol 12(4):390–401

    PubMed  Google Scholar 

  55. Clark RA (1993) Regulation of fibroplasia in cutaneous wound repair. Am J Med Sci 306(1):42–48

    CAS  PubMed  Google Scholar 

  56. McNeil PL, Kirchhausen T (2005) An emergency response team for membrane repair. Nat Rev Mol Cell Biol 6(6):499–505

    CAS  PubMed  Google Scholar 

  57. Roy S et al (2008) Characterization of the acute temporal changes in excisional murine cutaneous wound inflammation by screening of the wound-edge transcriptome. Physiol Genom 34(2):162–184

    CAS  Google Scholar 

  58. Cheng C-F et al (2008) Profiling motility signal-specific genes in primary human keratinocytes. J Investig Dermatol 128(8):1981–1990

    CAS  PubMed  Google Scholar 

  59. Ito M et al (2007) Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447(7142):316–320

    CAS  PubMed  Google Scholar 

  60. Becker CM, D’Amato RJ (2007) Angiogenesis and antiangiogenic therapy in endometriosis. Microvasc Res 74(2–3):121–130

    CAS  PubMed  Google Scholar 

  61. May K, Becker C (2008) Endometriosis and angiogenesis. Minerva Ginecol 60(3):245–254

    CAS  PubMed  Google Scholar 

  62. Sourial S, Tempest N, Hapangama DK (2014) Theories on the pathogenesis of endometriosis. Int J Reprod Med 2014:1–9

    Google Scholar 

  63. Witz CA (2002) Pathogenesis of endometriosis. Gynecol Obstet Investig 53(Suppl. 1):52–62

    Google Scholar 

  64. McLaren J et al (1996) Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis. Hum Reprod 11(1):220–223

    CAS  PubMed  Google Scholar 

  65. Mueller MD et al (2000) Neutrophils infiltrating the endometrium express vascular endothelial growth factor: potential role in endometrial angiogenesis. Fertil Steril 74(1):107–112

    CAS  PubMed  Google Scholar 

  66. Hyder SM et al (2000) Identification of functional estrogen response elements in the gene coding for the potent angiogenic factor vascular endothelial growth factor. Cancer Res 60(12):3183–3190

    CAS  PubMed  Google Scholar 

  67. Hull ML et al (2003) Antiangiogenic agents are effective inhibitors of endometriosis. J Clin Endocrinol Metab 88(6):2889–2899

    CAS  PubMed  Google Scholar 

  68. Folkman J (1974) Tumor angiogenesis factor. Can Res 34(8):2109–2113

    CAS  Google Scholar 

  69. Kerbel RS (2006) Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science 312(5777):1171–1175

    CAS  PubMed  Google Scholar 

  70. Al-Husein B et al (2012) Antiangiogenic therapy for cancer: an update. Pharmacother J Hum Pharmacol Drug Ther 32(12):1095–1111

    CAS  Google Scholar 

  71. Gupta K, Zhang J (2005) Angiogenesis: a curse or cure? Postgrad Med J 81(954):236–242

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Cines DB et al (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood J Am Soc Hematol 91(10):3527–3561

    CAS  Google Scholar 

  73. Sennino B et al (2007) Sequential loss of tumor vessel pericytes and endothelial cells after inhibition of platelet-derived growth factor B by selective aptamer AX102. Can Res 67(15):7358–7367

    CAS  Google Scholar 

  74. Griffioen AW, Molema G (2000) Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol Rev 52(2):237–268

    CAS  PubMed  Google Scholar 

  75. Murohara T et al (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Investig 101(11):2567–2578

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Pandya NM, Dhalla NS, Santani DD (2006) Angiogenesis—a new target for future therapy. Vasc Pharmacol 44(5):265–274

    CAS  Google Scholar 

  77. Furuya M, Yonemitsu Y (2008) Cancer neovascularization and proinflammatory microenvironments. Curr Cancer Drug Targets 8(4):253–265

    CAS  PubMed  Google Scholar 

  78. Furuya M et al (2005) Pathophysiology of tumor neovascularization. Vasc Health Risk Manag Healthc Policy 1(4):277

    CAS  Google Scholar 

  79. Ribatti D et al (2007) The structure of the vascular network of tumors. Cancer Lett 248(1):18–23

    CAS  PubMed  Google Scholar 

  80. Croix BS et al (2000) Genes expressed in human tumor endothelium. Science 289(5482):1197–1202

    Google Scholar 

  81. Parker BS et al (2004) Alterations in vascular gene expression in invasive breast carcinoma. Can Res 64(21):7857–7866

    CAS  Google Scholar 

  82. Madden SL et al (2004) Vascular gene expression in nonneoplastic and malignant brain. Am J Pathol 165(2):601–608

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Dvorak H (2005) Angiogenesis: update 2005. J Thromb Haemost 3(8):1835–1842

    CAS  PubMed  Google Scholar 

  84. Rajabi M, Mousa SA (2017) The role of angiogenesis in cancer treatment. Biomedicines 5(2):34

    PubMed Central  Google Scholar 

  85. Hirakawa S et al (2005) VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 201(7):1089–1099

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Nishida N et al (2006) Angiogenesis in cancer. Vasc Health Risk Manag Healthc Policy 2(3):213

    CAS  Google Scholar 

  87. Marneros AG (2009) Tumor angiogenesis in melanoma. Hematol Oncol Clin 23(3):431–446

    Google Scholar 

  88. Martin MJ et al (2012) Metformin accelerates the growth of BRAFV600E-driven melanoma by upregulating VEGF-A. Cancer Discov 2(4):344–355

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Stec M et al (2015) Isolation and characterization of circulating micro (nano) vesicles in the plasma of colorectal cancer patients and their interactions with tumor cells. Oncol Rep 34(5):2768–2775

    CAS  PubMed  Google Scholar 

  90. Olejarz W, Łacheta D, Kubiak-Tomaszewska G (2020) Matrix metalloproteinases as biomarkers of atherosclerotic plaque instability. Int J Mol Sci 21(11):3946

    CAS  PubMed Central  Google Scholar 

  91. Skog J et al (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10(12):1470–1476

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Kanninen KM et al (2016) Exosomes as new diagnostic tools in CNS diseases. Biochim Biophys Acta Mol Basis Dis 1862(3):403–410

    CAS  Google Scholar 

  93. Esa A et al (2019) Extracellular vesicles in the synovial joint: is there a role in the pathophysiology of osteoarthritis? Malays Orthop J 13(1):1

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Zeng Y et al (2019) Anti-angiogenesis triggers exosomes release from endothelial cells to promote tumor vasculogenesis. J Extracell Vesicles 8(1):1629865

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Whiteside TL (2016) Tumor-derived exosomes and their role in cancer progression. Adv Clin Chem 74:103–141

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Huang A et al (2015) Exosomal transfer of vasorin expressed in hepatocellular carcinoma cells promotes migration of human umbilical vein endothelial cells. Int J Biol Sci 11(8):961

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Qu L et al (2016) Exosome-transmitted lncARSR promotes sunitinib resistance in renal cancer by acting as a competing endogenous RNA. Cancer Cell 29(5):653–668

    CAS  PubMed  Google Scholar 

  98. Yeo RWY et al (2013) Mesenchymal stem cell: an efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev 65(3):336–341

    CAS  PubMed  Google Scholar 

  99. Chen B et al (2019) Human embryonic stem cell-derived exosomes promote pressure ulcer healing in aged mice by rejuvenating senescent endothelial cells. Stem Cell Res 10(1):1–17

    Google Scholar 

  100. Waltenberger J (2007) New horizons in diabetes therapy: the angiogenesis paradox in diabetes: description of the problem and presentation of a unifying hypothesis. Immunol Endocr Metab Agents Med Chem 7(1):87–93

    CAS  Google Scholar 

  101. Martin A, Komada MR, Sane DC (2003) Abnormal angiogenesis in diabetes mellitus. Med Res Rev 23(2):117–145

    CAS  PubMed  Google Scholar 

  102. Cheng R, Ma J-X (2015) Angiogenesis in diabetes and obesity. Rev Endocr Metab Disord 16(1):67–75

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Okonkwo UA, DiPietro LA (2017) Diabetes and wound angiogenesis. Int J Mol Sci 18(7):1419

    PubMed Central  Google Scholar 

  104. Tomanek RJ, Schatteman GC (2000) Angiogenesis: new insights and therapeutic potential. Anat Rec 261(3):126–135

    CAS  PubMed  Google Scholar 

  105. Abacı A et al (1999) Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 99(17):2239–2242

    PubMed  Google Scholar 

  106. Werner GS et al (2001) Collateral function in chronic total coronary occlusions is related to regional myocardial function and duration of occlusion. Circulation 104(23):2784–2790

    CAS  PubMed  Google Scholar 

  107. Tan S et al (2021) Differences of angiogenesis factors in tumor and diabetes mellitus. Diabetes Metab Syndr Obes Targets Ther 14:3375

    Google Scholar 

  108. Kolluru GK, Bir SC, Kevil CG (2012) Endothelial dysfunction and diabetes: effects on angiogenesis, vascular remodeling, and wound healing. Int J Vasc Med 2012:1–30

    Google Scholar 

  109. Chung AS, Ferrara N (2011) Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol (New York, N.Y.: 1985) 27:563–584

    CAS  Google Scholar 

  110. Humar R, Zimmerli L, Battegay E (2009) Angiogenesis and hypertension: an update. J Hum Hypertens 23(12):773–782

    CAS  PubMed  Google Scholar 

  111. Ferroni P et al (2012) Angiogenesis and hypertension: the dual role of anti-hypertensive and anti-angiogenic therapies. Curr Vasc Pharmacol 10(4):479–493

    CAS  PubMed  Google Scholar 

  112. Yang JC et al (2003) A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349(5):427–434

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Felmeden DC et al (2003) Endothelial damage and angiogenesis in hypertensive patients: relationship to cardiovascular risk factors and risk factor management. Am J Hypertens 16(1):11–20

    CAS  PubMed  Google Scholar 

  114. Sane DC, Anton L, Brosnihan KB (2004) Angiogenic growth factors and hypertension. Angiogenesis 7(3):193–201

    CAS  PubMed  Google Scholar 

  115. Yang R et al (2002) Exaggerated hypotensive effect of vascular endothelial growth factor in spontaneously hypertensive rats. Hypertension 39(3):815–820

    CAS  PubMed  Google Scholar 

  116. Vila V et al (2008) Inflammation, endothelial dysfunction and angiogenesis markers in chronic heart failure patients. Int J Cardiol 130(2):276–277

    PubMed  Google Scholar 

  117. Kiefer FN et al (2004) A versatile in vitro assay for investigating angiogenesis of the heart. Exp Cell Res 300(2):272–282

    CAS  PubMed  Google Scholar 

  118. Grass TM, Lurie DI, Coffin JD (2006) Transitional angiogenesis and vascular remodeling during coronary angiogenesis in response to myocardial infarction. Acta Histochem 108(4):293–302

    PubMed  Google Scholar 

  119. Rouwkema J, Rivron NC, van Blitterswijk CA (2008) Vascularization in tissue engineering. Trends Biotechnol 26(8):434–441

    CAS  PubMed  Google Scholar 

  120. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8(6):464–478

    CAS  PubMed  Google Scholar 

  121. Kaully T et al (2009) Vascularization—the conduit to viable engineered tissues. Tissue Eng Part B Rev 15(2):159–169

    CAS  PubMed  Google Scholar 

  122. Birla R (2014) Introduction to tissue engineering: applications and challenges. Wiley, Hoboken

    Google Scholar 

  123. Atluri P, Woo YJ (2008) Pro-angiogenic cytokines as cardiovascular therapeutics. BioDrugs 22(4):209–222

    CAS  PubMed  Google Scholar 

  124. Wang Y et al (2018) New insights into the regulatory role of microRNA in tumor angiogenesis and clinical implications. Mol Cancer 17(1):1–10

    Google Scholar 

  125. Ferrara N, Gerber H-P, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669–676

    CAS  PubMed  Google Scholar 

  126. Carmeliet P (2005) VEGF as a key mediator of angiogenesis in cancer. Oncology 69(Suppl. 3):4–10

    CAS  PubMed  Google Scholar 

  127. George ML et al (2001) Vegf-a, vegf-c, and vegf-d in colorectal cancer progression. Neoplasia 3(5):420–427

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Struman I et al (1999) Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. Proc Natl Acad Sci 96(4):1246–1251

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Hoeben A et al (2004) Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 56(4):549–580

    CAS  PubMed  Google Scholar 

  130. Rissanen TT et al (2003) VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ Res 92(10):1098–1106

    CAS  PubMed  Google Scholar 

  131. Zhao H-C et al (2006) Microvessel density is a prognostic marker of human gastric cancer. World J Gastroenterol WJG 12(47):7598

    PubMed  Google Scholar 

  132. Huwer H et al (2001) Simultaneous surgical revascularization and angiogenic gene therapy in diffuse coronary artery disease. Eur J Cardiothorac Surg 20(6):1128–1134

    CAS  PubMed  Google Scholar 

  133. Celik T et al (2005) Impaired coronary collateral vessel development in patients with proliferative diabetic retinopathy. Clin Cardiol Int Index Peer Rev J Adv Treat Cardiovasc Dis 28(8):384–388

    Google Scholar 

  134. Chou E et al (2002) Decreased cardiac expression of vascular endothelial growth factor and its receptors in insulin-resistant and diabetic States: a possible explanation for impaired collateral formation in cardiac tissue. Circulation 105(3):373–379

    CAS  PubMed  Google Scholar 

  135. Aiello LP, Wong J-S (2000) Role of vascular endothelial growth factor in diabetic vascular complications. Kidney Int 58:S113–S119

    Google Scholar 

  136. Chen S, Ziyadeh FN (2008) Vascular endothelial growth factor and diabetic nephropathy. Curr Diabetes Rep 8(6):470–476

    Google Scholar 

  137. Raab S, Plate KH (2007) Different networks, common growth factors: shared growth factors and receptors of the vascular and the nervous system. Acta Neuropathol 113(6):607–626

    CAS  PubMed  Google Scholar 

  138. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9(6):653–660

    CAS  PubMed  Google Scholar 

  139. Hall H (2007) Modified fibrin hydrogel matrices: both, 3D-scaffolds and local and controlled release systems to stimulate angiogenesis. Curr Pharm Des 13(35):3597–3607

    CAS  PubMed  Google Scholar 

  140. Peng S et al (2021) LncRNA-AK137033 inhibits the osteogenic potential of adipose-derived stem cells in diabetic osteoporosis by regulating Wnt signaling pathway via DNA methylation. Cell Prolif 55:e13174

    PubMed  PubMed Central  Google Scholar 

  141. Son J et al (2019) DNA aptamer immobilized hydroxyapatite for enhancing angiogenesis and bone regeneration. Acta Biomater 99:469–478

    CAS  PubMed  Google Scholar 

  142. Hardy B et al (2007) Angiogenesis induced by novel peptides selected from a phage display library by screening human vascular endothelial cells under different physiological conditions. Peptides 28(3):691–701

    CAS  PubMed  Google Scholar 

  143. Cavanagh PR et al (2005) Treatment for diabetic foot ulcers. Lancet 366(9498):1725–1735

    PubMed  Google Scholar 

  144. Van Hove AH, Benoit DS (2015) Depot-based delivery systems for pro-angiogenic peptides: a review. Front Bioeng Biotechnol Adv 3:102

    Google Scholar 

  145. Pickart L (2008) The human tri-peptide GHK and tissue remodeling. J Biomater Sci Polym Ed 19(8):969–988

    CAS  PubMed  Google Scholar 

  146. Akeson AL et al (1996) AF12198, a novel low molecular weight antagonist, selectively binds the human type I interleukin (IL)-1 receptor and blocks in vivo responses to IL-1. J Biol Chem 271(48):30517–30523

    CAS  PubMed  Google Scholar 

  147. Mandrup-Poulsen T (2012) Interleukin-1 antagonists and other cytokine blockade strategies for type 1 diabetes. Rev Diabet Stud RDS 9(4):338

    PubMed  Google Scholar 

  148. Olsson A-K et al (2004) The minimal active domain of endostatin is a heparin-binding motif that mediates inhibition of tumor vascularization. Can Res 64(24):9012–9017

    CAS  Google Scholar 

  149. Chew CK, Clarke BL (2017) Abaloparatide: recombinant human PTHrP (1–34) anabolic therapy for osteoporosis. Maturitas 97:53–60

    CAS  PubMed  Google Scholar 

  150. Zhanel GG, Schweizer F, Karlowsky JA (2012) Oritavancin: mechanism of action. Clin Infect Dis 54(suppl_3):S214–S219

    CAS  PubMed  Google Scholar 

  151. Finetti F et al (2012) Functional and pharmacological characterization of a VEGF mimetic peptide on reparative angiogenesis. Biochem Pharmacol 84(3):303–311

    CAS  PubMed  Google Scholar 

  152. Slyke P, Dumont D (2011) Multimeric TIE 2 agonists and uses thereof in stimulating angiogenesis. USA Patent Application.

  153. Demidova-Rice TN, Geevarghese A, Herman IM (2011) Bioactive peptides derived from vascular endothelial cell extracellular matrices promote microvascular morphogenesis and wound healing in vitro. Wound Repair Regen 19(1):59–70

    PubMed  Google Scholar 

  154. Demidova-Rice TN et al (2012) Human platelet-rich plasma-and extracellular matrix-derived peptides promote impaired cutaneous wound healing in vivo. PLoS One 7(2):e32146

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Licht T et al (2003) Induction of pro-angiogenic signaling by a synthetic peptide derived from the second intracellular loop of S1P3 (EDG3). Blood 102(6):2099–2107

    CAS  PubMed  Google Scholar 

  156. Soro S et al (2008) A proangiogenic peptide derived from vascular endothelial growth factor receptor-1 acts through α5β1 integrin. Blood J Am Soc Hematol 111(7):3479–3488

    CAS  Google Scholar 

  157. Liu J-M et al (2003) The tetrapeptide AcSDKP, an inhibitor of primitive hematopoietic cell proliferation, induces angiogenesis in vitro and in vivo. Blood J Am Soc Hematol 101(8):3014–3020

    CAS  Google Scholar 

  158. Gao N et al (2002) Vanadate-induced expression of hypoxia-inducible factor 1α and vascular endothelial growth factor through phosphatidylinositol 3-kinase/Akt pathway and reactive oxygen species. J Biol Chem 277(35):31963–31971

    CAS  PubMed  Google Scholar 

  159. Nishio S et al (2008) Cap43/NDRG1/Drg-1 is a molecular target for angiogenesis and a prognostic indicator in cervical adenocarcinoma. Cancer Lett 264(1):36–43

    CAS  PubMed  Google Scholar 

  160. Chua M-S et al (2007) Overexpression of NDRG1 is an indicator of poor prognosis in hepatocellular carcinoma. Mod Pathol 20(1):76–83

    CAS  PubMed  Google Scholar 

  161. Mousa SA et al (2007) Pro-angiogenesis action of arsenic and its reversal by selenium-derived compounds. Carcinogenesis 28(5):962–967

    CAS  PubMed  Google Scholar 

  162. Raines AL et al (2010) Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy. Biomaterials 31(18):4909–4917

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Zhai W et al (2012) Silicate bioceramics induce angiogenesis during bone regeneration. Acta Biomater 8(1):341–349

    CAS  PubMed  Google Scholar 

  164. Li H, Chang J (2013) Bioactive silicate materials stimulate angiogenesis in fibroblast and endothelial cell co-culture system through paracrine effect. Acta Biomater 9(6):6981–6991

    CAS  PubMed  Google Scholar 

  165. Das S et al (2012) The induction of angiogenesis by cerium oxide nanoparticles through the modulation of oxygen in intracellular environments. Biomaterials 33(31):7746–7755

    CAS  PubMed  PubMed Central  Google Scholar 

  166. Chachami G et al (2004) Cobalt induces hypoxia-inducible factor-1α expression in airway smooth muscle cells by a reactive oxygen species—and PI3K-dependent mechanism. Am J Respir Cell Mol Biol Evol 31(5):544–551

    CAS  Google Scholar 

  167. Bracken C, Whitelaw M, Peet D (2003) The hypoxia-inducible factors: key transcriptional regulators of hypoxic responses. Cell Mol Life Sci 60(7):1376–1393

    CAS  PubMed  Google Scholar 

  168. Bollu VS et al (2016) Evaluation of in vivo cytogenetic toxicity of europium hydroxide nanorods (EHNs) in male and female Swiss albino mice. ACS Biomater Sci 10(4):413–425

    CAS  Google Scholar 

  169. Ge K et al (2016) Europium-doped NaYF 4 nanoparticles cause the necrosis of primary mouse bone marrow stromal cells through lysosome damage. RSC Adv 6(26):21725–21734

    CAS  Google Scholar 

  170. Papapetropoulos A et al (2009) Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc Natl Acad Sci 106(51):21972–21977

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Coletta C et al (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc Natl Acad Sci 109(23):9161–9166

    CAS  PubMed  PubMed Central  Google Scholar 

  172. Mao CD, Hoang P, DiCorleto PE (2001) Lithium inhibits cell cycle progression and induces stabilization of p53 in bovine aortic endothelial cells. J Biol Chem 276(28):26180–26188

    CAS  PubMed  Google Scholar 

  173. Nethi SK et al (2017) Pro-angiogenic properties of terbium hydroxide nanorods: molecular mechanisms and therapeutic applications in wound healing. ACS Biomater Sci Eng Min J 3(12):3635–3645

    CAS  Google Scholar 

  174. Augustine R et al (2019) Yttrium oxide nanoparticle loaded scaffolds with enhanced cell adhesion and vascularization for tissue engineering applications. Mater Sci Eng C 103:109801

    CAS  Google Scholar 

  175. Boehm T et al (1998) Zinc-binding of endostatin is essential for its antiangiogenic activity. Biochem Biophys Res Commun 252(1):190–194

    CAS  PubMed  Google Scholar 

  176. Ding Y-H et al (1998) Zinc-dependent dimers observed in crystals of human endostatin. Proc Natl Acad Sci 95(18):10443–10448

    CAS  PubMed  PubMed Central  Google Scholar 

  177. Loboda A et al (2008) Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 10(10):1767–1812

    CAS  PubMed  Google Scholar 

  178. Gullino P (1986) Considerations on the mechanism of the angiogenic response. Anticancer Res 6(2):153–158

    CAS  PubMed  Google Scholar 

  179. Raju KS et al (1982) Ceruloplasmin, copper ions, and angiogenesis. J Natl Cancer Inst 69(5):1183–1188

    CAS  PubMed  Google Scholar 

  180. Kohn EC et al (1995) Angiogenesis: role of calcium-mediated signal transduction. Proc Natl Acad Sci 92(5):1307–1311

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Dzondo-Gadet M et al (2002) Action of boron at the molecular level. Biol Trace Elem Res 85(1):23–33

    CAS  PubMed  Google Scholar 

  182. Bernardini D et al (2005) Magnesium and microvascular endothelial cells: a role in inflammation and angiogenesis. Front Biosci 10(1–3):1177–1182

    CAS  PubMed  Google Scholar 

  183. Miguez-Pacheco V et al (2018) Development and characterization of niobium-releasing silicate bioactive glasses for tissue engineering applications. J Eur Ceram Soc 38(3):871–876

    CAS  Google Scholar 

  184. Malhotra A, Habibovic P (2016) Calcium phosphates and angiogenesis: implications and advances for bone regeneration. Trends Biotechnol 34(12):983–992

    CAS  PubMed  Google Scholar 

  185. Liang H-C et al (2005) Loading of a novel angiogenic agent, ginsenoside Rg1 in an acellular biological tissue for tissue regeneration. Tissue Eng 11(5–6):835–846

    CAS  PubMed  Google Scholar 

  186. Yue PY et al (2005) Elucidation of the mechanisms underlying the angiogenic effects of ginsenoside Rg 1 in vivo and in vitro. Angiogenesis 8(3):205–216

    CAS  PubMed  Google Scholar 

  187. Sengupta S et al (2004) Modulating angiogenesis: the yin and the yang in ginseng. Circulation 110(10):1219–1225

    CAS  PubMed  Google Scholar 

  188. Hong SJ et al (2009) Angiogenic effect of saponin extract from Panax notoginseng on HUVECs in vitro and zebrafish in vivo. Phytother Res Int J Devot Pharmacol Toxicol Eval Nat Prod Deriv 23(5):677–686

    CAS  Google Scholar 

  189. Huang Y-C et al (2005) A natural compound (ginsenoside Re) isolated from Panax ginseng as a novel angiogenic agent for tissue regeneration. Pharm Res 22(4):636–646

    CAS  PubMed  Google Scholar 

  190. Xin X et al (2006) Extraction of 20 (S)-ginsenoside Rg2 from cultured Panax notoginseng cells in vitro stimulates human umbilical cord vein endothelial cell proliferation. Am J Ther 13(3):205–210

    PubMed  Google Scholar 

  191. Choi S et al (2002) Angiogenic activity of β-sitosterol in the ischaemia/reperfusion-damaged brain of Mongolian gerbil. Planta Med 68(04):330–335

    CAS  PubMed  Google Scholar 

  192. Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77(7):527–543

    CAS  PubMed  Google Scholar 

  193. Meng H et al (2008) Angiogenic effects of the extracts from Chinese herbs: Angelica and Chuanxiong. Am J Chin Med 36(03):541–554

    CAS  PubMed  Google Scholar 

  194. Lam HW et al (2008) The angiogenic effects of Angelica sinensis extract on HUVEC in vitro and zebrafish in vivo. J Cell Biochem 103(1):195–211

    CAS  PubMed  Google Scholar 

  195. Zhang Y et al (2009) Radix Astragali extract promotes angiogenesis involving vascular endothelial growth factor receptor-related phosphatidylinositol 3-kinase/Akt-dependent pathway in human endothelial cells. Phytother Res Int J Devot Pharmacol Toxicol Eval Nat Prod Deriv 23(9):1205–1213

    CAS  Google Scholar 

  196. Zheng KY et al (2011) Flavonoids from Radix Astragali induce the expression of erythropoietin in cultured cells: a signaling mediated via the accumulation of hypoxia-inducible factor-1α. J Agric Food Chem 59(5):1697–1704

    CAS  PubMed  Google Scholar 

  197. Choi D-Y et al (2009) Stimulatory effect of Cinnamomum cassia and cinnamic acid on angiogenesis through up-regulation of VEGF and Flk-1/KDR expression. Int Immunopharmacol 9(7–8):959–967

    CAS  PubMed  Google Scholar 

  198. Chen H et al (2012) Reconstitution of coronary vasculature in ischemic hearts by plant-derived angiogenic compounds. Int J Cardiol 156(2):148–155

    PubMed  Google Scholar 

  199. Zhang Q et al (2021) Tetrahedral framework nucleic acids act as antioxidants in acute kidney injury treatment. Chem Eng J 413:127426

    CAS  Google Scholar 

  200. Zhang T et al (2020) Design, fabrication and applications of tetrahedral DNA nanostructure-based multifunctional complexes in drug delivery and biomedical treatment. Nat Protoc 15(8):2728–2757

    CAS  PubMed  Google Scholar 

  201. Liu Y et al (2020) Tetrahedral framework nucleic acids deliver antimicrobial peptides with improved effects and less susceptibility to bacterial degradation. Nano Lett 20(5):3602–3610

    CAS  PubMed  Google Scholar 

  202. Yoshitomi T et al (2020) Binding and structural properties of DNA aptamers with VEGF-A-mimic activity. Mol Ther Nucleic Acids 19:1145–1152

    CAS  PubMed  PubMed Central  Google Scholar 

  203. Nonaka Y et al (2013) Affinity improvement of a VEGF aptamer by in silico maturation for a sensitive VEGF-detection system. Anal Chem 85(2):1132–1137

    CAS  PubMed  Google Scholar 

  204. Zhao D et al (2020) Tetrahedral framework nucleic acid promotes the treatment of bisphosphonate-related osteonecrosis of the jaws by promoting angiogenesis and M2 polarization. ACS Appl Mater Interfaces 12(40):44508–44522

    CAS  PubMed  Google Scholar 

  205. Lin S et al (2020) Antioxidative and angiogenesis-promoting effects of tetrahedral framework nucleic acids in diabetic wound healing with activation of the Akt/Nrf2/HO-1 pathway. ACS Appl Mater Interfaces 12(10):11397–11408

    CAS  PubMed  Google Scholar 

  206. Juhl O IV et al (2019) Aptamer-functionalized fibrin hydrogel improves vascular endothelial growth factor release kinetics and enhances angiogenesis and osteogenesis in critically sized cranial defects. ACS Biomater Sci Eng Min J 5(11):6152–6160

    CAS  Google Scholar 

  207. Khademhosseini A, Vacanti JP, Langer R (2009) Progress in tissue engineering. Sci Am 300(5):64–71

    CAS  PubMed  Google Scholar 

  208. Song H-HG et al (2018) Vascular tissue engineering: progress, challenges, and clinical promise. Cell Stem Cell 22(3):340–354

    CAS  PubMed  PubMed Central  Google Scholar 

  209. Ravi S, Chaikof EL (2010) Biomaterials for vascular tissue engineering. Regen Med 5(1):107–120

    CAS  PubMed  Google Scholar 

  210. Lovett M et al (2009) Vascularization strategies for tissue engineering. Tissue Eng Part B Rev 15(3):353–370

    CAS  PubMed  PubMed Central  Google Scholar 

  211. Li S, Sengupta D, Chien S (2014) Vascular tissue engineering: from in vitro to in situ. Wiley Interdiscip Rev Syst Biol Med Glob Surviv 6(1):61–76

    CAS  Google Scholar 

  212. Leal BB et al (2021) Vascular tissue engineering: polymers and methodologies for small caliber vascular grafts. Front Cardiovasc Med 7:376

    Google Scholar 

  213. Liu Y, Chan-Park MB (2009) Hydrogel based on interpenetrating polymer networks of dextran and gelatin for vascular tissue engineering. Biomaterials 30(2):196–207

    PubMed  Google Scholar 

  214. Ma H, Hu J, Ma PX (2010) Polymer scaffolds for small-diameter vascular tissue engineering. Adv Func Mater 20(17):2833–2841

    CAS  Google Scholar 

  215. Johnstone RW, Ruefli AA, Lowe SW (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108(2):153–164

    CAS  PubMed  Google Scholar 

  216. Kerbel R, Folkman J (2002) Clinical translation of angiogenesis inhibitors. Nat Rev Cancer 2(10):727–739

    CAS  PubMed  Google Scholar 

  217. Makrilia N et al (2009) The role of angiogenesis in solid tumours: an overview. Eur J Intern Med 20(7):663–671

    CAS  PubMed  Google Scholar 

  218. Gold L et al (2012) Aptamers and the RNA World, Past and Present. Cold Spring Harb Perspect Biol 4:a003582

    PubMed  PubMed Central  Google Scholar 

  219. Ribatti D (2009) Endogenous inhibitors of angiogenesis: a historical review. Leuk Res 33(5):638–644

    CAS  PubMed  Google Scholar 

  220. Kusaka M et al (1991) Potent anti-angiogenic action of AGM-1470: comparison to the fumagillin parent. Biochem Biophys Res Commun 174(3):1070–1076

    CAS  PubMed  Google Scholar 

  221. Gupta SK, Hassel T, Singh JP (1995) A potent inhibitor of endothelial cell proliferation is generated by proteolytic cleavage of the chemokine platelet factor 4. Proc Natl Acad Sci 92(17):7799–7803

    CAS  PubMed  PubMed Central  Google Scholar 

  222. Nasir A (2019) Angiogenic signaling pathways and anti-angiogenic therapies in human cancer. Predictive biomarkers in oncology. Springer, New York, pp 243–262

    Google Scholar 

  223. Wu J et al (2020) Synergic effect of PD-1 blockade and endostar on the PI3K/AKT/mTOR-mediated autophagy and angiogenesis in Lewis lung carcinoma mouse model. Biomed Pharmacother 125:109746

    CAS  PubMed  Google Scholar 

  224. O’Reilly MS et al (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79(2):315–328

    CAS  PubMed  Google Scholar 

  225. Streck CJ et al (2005) Interferon-mediated anti-angiogenic therapy for neuroblastoma. Cancer Lett 228(1–2):163–170

    CAS  PubMed  Google Scholar 

  226. Briukhovetska D et al (2021) Interleukins in cancer: from biology to therapy. Nat Rev Cancer 21:1–19

    Google Scholar 

  227. Lee G-R, Ahn M-R (2020) Inhibition of vascular endothelial growth factor-induced angiogenesis by bee products. Korean Society of Food and Nutrition, 430–431

  228. Goto F et al (1993) Synergistic effects of vascular endothelial growth factor and basic fibroblast growth factor on the proliferation and cord formation of bovine capillary endothelial cells within collagen gels. Lab Investig J Tech Methods 69(5):508–517

    CAS  Google Scholar 

  229. Li K, Tay FR, Yiu CKY (2020) The past, present and future perspectives of matrix metalloproteinase inhibitors. Pharmacol Ther Clin Risk Manag 207:107465

    CAS  Google Scholar 

  230. Shweiki D et al (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359(6398):843–845

    CAS  PubMed  Google Scholar 

  231. Davis S et al (1996) Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87(7):1161–1169

    CAS  PubMed  Google Scholar 

  232. Heljasvaara R et al (2005) Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp Cell Res 307(2):292–304

    CAS  PubMed  Google Scholar 

  233. Ortega N, Werb Z (2002) New functional roles for non-collagenous domains of basement membrane collagens. J Cell Sci 115(22):4201–4214

    CAS  PubMed  Google Scholar 

  234. Cook KM, Figg WD (2010) Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J Clin 60(4):222–243

    PubMed  PubMed Central  Google Scholar 

  235. Fayette J, Soria J-C, Armand J-P (2005) Use of angiogenesis inhibitors in tumour treatment. Eur J Cancer 41(8):1109–1116

    CAS  PubMed  Google Scholar 

  236. Margolin K et al (2001) Phase Ib trial of intravenous recombinant humanized monoclonal antibody to vascular endothelial growth factor in combination with chemotherapy in patients with advanced cancer: pharmacologic and long-term safety data. J Clin Oncol 19(3):851–856

    CAS  PubMed  Google Scholar 

  237. Reichert J et al (2010) Development trends for peptide therapeutics. Peptide Therapeutics Foundation

  238. Saladin PM, Zhang BD, Reichert JM (2009) Current trends in the clinical development of peptide therapeutics. IDrugs Investig Drugs J 12(12):779–784

    CAS  Google Scholar 

  239. Bhutia SK, Maiti TK (2008) Targeting tumors with peptides from natural sources. Trends Biotechnol 26(4):210–217

    CAS  PubMed  Google Scholar 

  240. Rosca VE et al (2011) Anti-angiogenic peptides for cancer therapeutics. Curr Pharm Biotechnol 12(8):1101–1116

    CAS  PubMed  PubMed Central  Google Scholar 

  241. Thevenard J et al (2006) Structural and antitumor properties of the YSNSG cyclopeptide derived from tumstatin. Chem Biol Philos 13(12):1307–1315

    CAS  Google Scholar 

  242. Park K et al (2008) Tumor endothelial cell targeted cyclic RGD-modified heparin derivative: inhibition of angiogenesis and tumor growth. Pharm Res 25(12):2786–2798

    CAS  PubMed  Google Scholar 

  243. Doñate F et al (2008) Pharmacology of the novel antiangiogenic peptide ATN-161 (Ac-PHSCN-NH2): observation of a U-shaped dose-response curve in several preclinical models of angiogenesis and tumor growth. Clin Cancer Res 14(7):2137–2144

    PubMed  Google Scholar 

  244. Hariharan S et al (2007) Assessment of the biological and pharmacological effects of the ανβ3 and ανβ5 integrin receptor antagonist, cilengitide (EMD 121974), in patients with advanced solid tumors. Ann Oncol 18(8):1400–1407

    CAS  PubMed  Google Scholar 

  245. Reardon DA et al (2007) Randomized phase II study of cilengitide, an integrin-targeting arginine-glycine-aspartic acid peptide, in recurrent glioblastoma multiforme. Clin Oncol 26:5610–5617

    Google Scholar 

  246. Giordano RJ et al (2010) From combinatorial peptide selection to drug prototype (I): targeting the vascular endothelial growth factor receptor pathway. Proc Natl Acad Sci 107(11):5112–5117

    CAS  PubMed  PubMed Central  Google Scholar 

  247. Juarez JC et al (2002) Histidine-proline-rich glycoprotein has potent antiangiogenic activity mediated through the histidine-proline-rich domain. Can Res 62(18):5344–5350

    CAS  Google Scholar 

  248. Dixelius J et al (2006) Minimal active domain and mechanism of action of the angiogenesis inhibitor histidine-rich glycoprotein. Can Res 66(4):2089–2097

    CAS  Google Scholar 

  249. Guo Y et al (2002) An antiangiogenic urokinase-derived peptide combined with tamoxifen decreases tumor growth and metastasis in a syngeneic model of breast cancer. Can Res 62(16):4678–4684

    CAS  Google Scholar 

  250. Mishima K et al (2000) A peptide derived from the non-receptor-binding region of urokinase plasminogen activator inhibits glioblastoma growth and angiogenesis in vivo in combination with cisplatin. Proc Natl Acad Sci 97(15):8484–8489

    CAS  PubMed  PubMed Central  Google Scholar 

  251. Haviv F et al (2005) Thrombospondin-1 mimetic peptide inhibitors of angiogenesis and tumor growth: design, synthesis, and optimization of pharmacokinetics and biological activities. J Med Chem 48(8):2838–2846

    CAS  PubMed  Google Scholar 

  252. Ni S et al (2020) Recent progress in aptamer discoveries and modifications for therapeutic applications. ACS Appl Mater Interfaces 13(8):9500–9519

    PubMed  Google Scholar 

  253. Li L et al (2021) Nucleic acid aptamers for molecular diagnostics and therapeutics: advances and perspectives. Angew Chem Int Ed 60(5):2221–2231

    CAS  Google Scholar 

  254. Liu Y et al (2021) Immobilization strategies for enhancing sensitivity of electrochemical aptamer-based sensors. ACS Appl Mater Interfaces 13(8):9491–9499

    CAS  PubMed  PubMed Central  Google Scholar 

  255. McConnell EM, Nguyen J, Li Y (2020) Aptamer-based biosensors for environmental monitoring. Front Chem 8:434

    CAS  PubMed  PubMed Central  Google Scholar 

  256. Schmitz FRW et al (2020) An overview and future prospects on aptamers for food safety. Appl Microbiol Biotechnol Adv 104:1–11

    Google Scholar 

  257. Proske D et al (2005) Aptamers—basic research, drug development, and clinical applications. Appl Microbiol Biotechnol Adv 69(4):367–374

    CAS  Google Scholar 

  258. Carrasquillo KG et al (2003) Controlled delivery of the anti-VEGF aptamer EYE001 with poly (lactic-co-glycolic) acid microspheres. Investig Ophthalmol Vis Sci 44(1):290–299

    Google Scholar 

  259. Drolet DW et al (2000) Pharmacokinetics and safety of an anti-vascular endothelial growth factor aptamer (NX1838) following injection into the vitreous humor of rhesus monkeys. Pharm Res 17(12):1503–1510

    CAS  PubMed  Google Scholar 

  260. Pietras K et al (2002) Inhibition of PDGF receptor signaling in tumor stroma enhances antitumor effect of chemotherapy. Can Res 62(19):5476–5484

    CAS  Google Scholar 

  261. Jaffe GJ et al (2016) A phase 1 study of intravitreous E10030 in combination with ranibizumab in neovascular age-related macular degeneration. Ophthalmology 123(1):78–85

    PubMed  Google Scholar 

  262. Matsuda Y et al (2019) Anti-angiogenic and anti-scarring dual action of an anti-fibroblast growth factor 2 aptamer in animal models of retinal disease. Mol Ther Nucleic Acids 17:819–828

    CAS  PubMed  PubMed Central  Google Scholar 

  263. Lu C et al (2010) Targeting pericytes with a PDGF-B aptamer in human ovarian carcinoma models. Cancer Biol Ther 9(3):176–182

    CAS  PubMed  Google Scholar 

  264. Tezuka-Kagajo M et al (2020) Development of human CBF1-targeting single-stranded DNA aptamers with antiangiogenic activity in vitro. Nucleic Acid Ther 30(6):365–378

    CAS  PubMed  Google Scholar 

  265. Jellinek D et al (1993) High-affinity RNA ligands to basic fibroblast growth factor inhibit receptor binding. Proc Natl Acad Sci 90(23):11227–11231

    CAS  PubMed  PubMed Central  Google Scholar 

  266. Ruckman J et al (1998) 2′-Fluoropyrimidine RNA-based aptamers to the 165-amino acid form of vascular endothelial growth factor (VEGF165): Inhibition of receptor binding and VEGF-induced vascular permeability through interactions requiring the exon 7-encoded domain. J Biol Chem 273(32):20556–20567

    CAS  PubMed  Google Scholar 

  267. White RR et al (2003) Inhibition of rat corneal angiogenesis by a nuclease-resistant RNA aptamer specific for angiopoietin-2. Proc Natl Acad Sci 100(9):5028–5033

    CAS  PubMed  PubMed Central  Google Scholar 

  268. Roy T, James BD, Allen JB (2021) Anti-VEGF-R2 aptamer and RGD peptide synergize in a bifunctional hydrogel for enhanced angiogenic potential. Macromol Biosci 21(2):2000337

    CAS  Google Scholar 

  269. Muller YA et al (1998) VEGF and the Fab fragment of a humanized neutralizing antibody: crystal structure of the complex at 2.4 Å resolution and mutational analysis of the interface. Structure 6(9):1153–1167

    CAS  PubMed  Google Scholar 

  270. Asano M, Yukita A, Suzuki H (1999) Wide spectrum of antitumor activity of a neutralizing monoclonal antibody to human vascular endothelial growth factor. Jpn J Cancer Res 90(1):93–100

    CAS  PubMed  PubMed Central  Google Scholar 

  271. Itatani Y et al (2018) Resistance to anti-angiogenic therapy in cancer—alterations to anti-VEGF pathway. Int J Mol Sci 19(4):1232

    PubMed Central  Google Scholar 

  272. McCormack PL, Keam SJ (2008) Bevacizumab. Drugs Soc 68(4):487–506

    CAS  Google Scholar 

  273. Muyldermans S (2013) Nanobodies: natural single-domain antibodies. Annu Rev Biochem 82:775–797

    CAS  PubMed  Google Scholar 

  274. Arezumand R et al (2017) Nanobodies as novel agents for targeting angiogenesis in solid cancers. Front Immunol 8:1746

    PubMed  PubMed Central  Google Scholar 

  275. Woods J et al (2008) Direct antiangiogenic actions of cadmium on human vascular endothelial cells. Toxicol In Vitro 22(3):643–651

    CAS  PubMed  Google Scholar 

  276. Prozialeck W, Edwards JR, Woods JM (2006) The vascular endothelium as a target of cadmium toxicity. Life Sci 79:1493–1506

    CAS  PubMed  Google Scholar 

  277. Das S et al (2020) Anti-angiogenic vanadium pentoxide nanoparticles for the treatment of melanoma and their in vivo toxicity study. Nanoscale 12(14):7604–7621

    CAS  PubMed  Google Scholar 

  278. Yang MH et al (2017) Anti-angiogenic effect of arsenic trioxide in lung cancer via inhibition of endothelial cell migration, proliferation and tube formation. Oncol Lett 14(3):3103–3109

    PubMed  PubMed Central  Google Scholar 

  279. Jo DH et al (2014) Anti-angiogenic effect of bare titanium dioxide nanoparticles on pathologic neovascularization without unbearable toxicity. Nanomed Nanotechnol Biol Med Glob Surviv 10(5):e1109–e1117

    Google Scholar 

  280. Jo DH et al (2012) Antiangiogenic effect of silicate nanoparticle on retinal neovascularization induced by vascular endothelial growth factor. Biomaterials 8(5):784–791

    CAS  Google Scholar 

  281. Kim JH et al (2011) The inhibition of retinal neovascularization by gold nanoparticles via suppression of VEGFR-2 activation. Biomaterials 32(7):1865–1871

    CAS  PubMed  Google Scholar 

  282. Yong JM et al (2022) ROS-mediated anti-angiogenic activity of cerium oxide nanoparticles in melanoma cells. ACS Biomater Sci Eng Min J 8:512–525

    CAS  Google Scholar 

  283. Norrby K, Mattsby-Baltzer I, Innocenti M, Tuneberg S (2001) Orally administered bovine lactoferrin systemically inhibits VEGF-mediated angiogenesis in the rat. Int J Cancer 91:236–240

    CAS  PubMed  Google Scholar 

  284. Bussolati B et al (2009) Anti-angiogenic properties of calcium trifluoroacetate. Microvasc Res 78(3):272–277

    CAS  PubMed  Google Scholar 

  285. Maier JA et al (2004) High concentrations of magnesium modulate vascular endothelial cell behaviour in vitro. Biochim Biophys Acta Mol Basis Dis 1689(1):6–12

    CAS  Google Scholar 

  286. Ichikawa H et al (2007) Anticancer drugs designed by mother nature: ancient drugs but modern targets. Curr Pharm Des 13(33):3400–3416

    CAS  PubMed  Google Scholar 

  287. Kruger EA et al (2001) Approaches to preclinical screening of antiangiogenic agents. In: Seminars in oncology. Elsevier, Amsterdam

  288. Adlercreutz H (1990) Western diet and Western diseases: some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Investig J Tech Methods 50(sup201):3–23

    Google Scholar 

  289. Donaldson MS (2004) Nutrition and cancer: a review of the evidence for an anti-cancer diet. Nutr J 3(1):1–21

    Google Scholar 

  290. Neal C et al (2006) Clinical aspects of natural anti-angiogenic drugs. Curr Drug Targets 7(3):371–383

    CAS  PubMed  Google Scholar 

  291. Oberlies NH, Kroll DJ (2004) Camptothecin and taxol: historic achievements in natural products research. J Nat Prod 67(2):129–135

    CAS  PubMed  Google Scholar 

  292. Fan T-P et al (2006) Angiogenesis: from plants to blood vessels. Trends Pharmacol Sci 27(6):297–309

    CAS  PubMed  Google Scholar 

  293. Wani MC et al (1971) Plant antitumor agents. VI. Isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 93(9):2325–2327

    CAS  PubMed  Google Scholar 

  294. Kingston D, Newman DJ (2007) Taxoids: cancer-fighting compounds from nature. Curr Opin Drug Discov Dev Change 10(2):130–144

    CAS  Google Scholar 

  295. Block G, Patterson B, Subar A (1992) Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 18(1):1–29

    CAS  PubMed  Google Scholar 

  296. Lekas A et al (2005) 147Association of hypoxia inducible factor-1A (HIF-1A), vascular endothelial growth factor (VEGF) and angiogenesis in benign prostate hyperplasia. Eur Urol Suppl 3(4):39

    Google Scholar 

  297. Wall ME et al (1966) Plant antitumor agents. I. The isolation and structure of camptothecin, a novel alkaloidal leukemia and tumor inhibitor from camptotheca acuminata1, 2. J Am Chem Soc 88(16):3888–3890

    CAS  Google Scholar 

  298. Clements MK et al (1999) Antiangiogenic potential of camptothecin and topotecan. Cancer Chemother Pharmacol Ther 44(5):411–416

    CAS  Google Scholar 

  299. Jiang J et al (2019) Combretastatin A4 nanodrug-induced MMP9 amplification boosts tumor-selective release of doxorubicin prodrug. Adv Mater 31(44):1904278

    CAS  Google Scholar 

  300. Nainwal LM et al (2019) Combretastatin-based compounds with therapeutic characteristics: a patent review. Expert Opin Ther Pat 29(9):703–731

    CAS  PubMed  Google Scholar 

  301. Seddigi ZS et al (2017) Recent advances in combretastatin based derivatives and prodrugs as antimitotic agents. MedChemComm 8(8):1592–1603

    CAS  PubMed  PubMed Central  Google Scholar 

  302. Fotsis T et al (1993) Genistein, a dietary-derived inhibitor of in vitro angiogenesis. Proc Natl Acad Sci 90(7):2690–2694

    CAS  PubMed  PubMed Central  Google Scholar 

  303. Javed Z et al (2021) Genistein as a regulator of signaling pathways and microRNAs in different types of cancers. Cancer Cell Int 21(1):1–12

    Google Scholar 

  304. Guo J et al (2021) Involvement of α7nAChR in the protective effects of genistein against β-amyloid-induced oxidative stress in neurons via a PI3K/Akt/Nrf2 pathway-related mechanism. Cell Mol Neurobiol 41(2):377–393

    CAS  PubMed  Google Scholar 

  305. Kucuk O (2020) Genistein in prostate cancer prevention and treatment. Multidiscip Digit Publ Inst Proc 40(1):49

    Google Scholar 

  306. Sarkar FH, Li YJ (2003) Soy isoflavones and cancer prevention: clinical science review. Cancer Investig 21(5):744–757

    CAS  Google Scholar 

  307. Rodriguez SK et al (2006) Green tea catechin, epigallocatechin-3-gallate, inhibits vascular endothelial growth factor angiogenic signaling by disrupting the formation of a receptor complex. Int J Cancer Prev 118(7):1635–1644

    CAS  Google Scholar 

  308. Lamy S, Gingras D, Béliveau R (2002) Green tea catechins inhibit vascular endothelial growth factor receptor phosphorylation. Can Res 62(2):381–385

    CAS  Google Scholar 

  309. Lee B-C et al (2004) The inhibitory effects of aqueous extract of Magnolia officinalis on human mesangial cell proliferation by regulation of platelet-derived growth factor-BB and transforming growth factor-β1 expression. J Pharmacol Sci 94(1):81–85

    CAS  PubMed  Google Scholar 

  310. Lv P et al (2020) Tea polyphenols inhibit the growth and angiogenesis of breast cancer xenografts in a mouse model. J Trad Chin Med Sci 7(2):141–147

    Google Scholar 

  311. Bahramrezaie M et al (2019) Effects of resveratrol on VEGF & HIF1 genes expression in granulosa cells in the angiogenesis pathway and laboratory parameters of polycystic ovary syndrome: a triple-blind randomized clinical trial. J Assist Reprod Genet 36(8):1701–1712

    PubMed  PubMed Central  Google Scholar 

  312. Sudha T et al (2020) Resveratrol and its nanoformulation attenuate growth and the angiogenesis of xenograft and orthotopic colon cancer models. Molecules 25(6):1412

    CAS  PubMed Central  Google Scholar 

  313. Fukuda S et al (2006) Resveratrol ameliorates myocardial damage by inducing vascular endothelial growth factor-angiogenesis and tyrosine kinase receptor Flk-1. Cell Biochem Biophys 44(1):43–49

    CAS  PubMed  Google Scholar 

  314. Zou J et al (2000) Effects of resveratrol on oxidative modification of human low density lipoprotein. Chin Med J 113(2):99–102

    CAS  PubMed  Google Scholar 

  315. Bhat KP, Kosmeder JW, Pezzuto JM (2001) Biological effects of resveratrol. Antioxid Redox Signal 3(6):1041–1064

    CAS  PubMed  Google Scholar 

  316. Guo R et al (2014) Resveratrol suppresses oxidised low-density lipoprotein-induced macrophage apoptosis through inhibition of intracellular reactive oxygen species generation, LOX-1, and the p38 MAPK pathway. Cell Physiol Biochem 34(2):603–616

    CAS  PubMed  Google Scholar 

  317. Petrovski G, Gurusamy N, Das DK (2011) Resveratrol in cardiovascular health and disease. Ann N Y Acad Sci 1215(1):22–33

    PubMed  Google Scholar 

  318. Liu X et al (2016) The effect and action mechanism of resveratrol on the vascular endothelial cell by high glucose treatment. Saudi J Biol Sci 23(1):S16–S21

    CAS  PubMed  Google Scholar 

  319. Gururaj AE et al (2002) Molecular mechanisms of anti-angiogenic effect of curcumin. Biochem Biophys Res Commun 297(4):934–942

    CAS  PubMed  Google Scholar 

  320. Arbiser JL et al (1998) Curcumin is an in vivo inhibitor of angiogenesis. Mol Med 4(6):376–383

    CAS  PubMed  PubMed Central  Google Scholar 

  321. Khafif A et al (2005) Curcumin: a new radio-sensitizer of squamous cell carcinoma cells. Otolaryngol Head Neck Surg 132(2):317–321

    PubMed  Google Scholar 

  322. Sen S, Sharma H, Singh N (2005) Curcumin enhances Vinorelbine mediated apoptosis in NSCLC cells by the mitochondrial pathway. Biochem Biophys Res Commun 331(4):1245–1252

    CAS  PubMed  Google Scholar 

  323. Upadhyay N et al (2021) Recent anti-angiogenic drug discovery efforts to combat cancer. ChemistrySelect 6(23):5689–5700

    CAS  Google Scholar 

  324. Al-Abd AM et al (2017) Anti-angiogenic agents for the treatment of solid tumors: potential pathways, therapy and current strategies—a review. J Adv Res 8(6):591–605

    CAS  PubMed  PubMed Central  Google Scholar 

  325. Cohen DJ, Giordano FJ, Hammond HK, Uham RX, Li W, Pike M, Sellke FW, Stegmann TJ, Udelson JE, Rosengartt TK (2000) Clinical trials in coronary angiogenesis: issues, problems, consensus: an expert panel summary. Circulation 102:E73-86

    PubMed  Google Scholar 

  326. Chibaudel B et al (2020) Association of bevacizumab plus oxaliplatin-based chemotherapy with disease-free survival and overall survival in patients with stage II colon cancer: a secondary analysis of the AVANT trial. JAMA Netw Open 3(10):e2020425–e2020425

    PubMed  PubMed Central  Google Scholar 

  327. de Castro Junior G et al (2006) Angiogenesis and cancer: a cross-talk between basic science and clinical trials (the “do ut des” paradigm). Crit Rev Oncol Hematol 59(1):40–50

    PubMed  Google Scholar 

  328. Casparini G et al (2005) Combination of antiangiogenic therapy with other anticancer therapies: results, challenges, and other questions. J Clin Oncol 23(6):1295–1311

    Google Scholar 

  329. Horstmann E et al (2005) Risks and benefits of phase 1 oncology trials, 1991 through 2002. N Engl J Med 352(9):895–904

    CAS  PubMed  Google Scholar 

  330. Hurwitz H et al (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350(23):2335–2342

    CAS  PubMed  Google Scholar 

  331. Kabbinavar FF et al (2005) Combined analysis of efficacy: the addition of bevacizumab to fluorouracil/leucovorin improves survival for patients with metastatic colorectal cancer. Eur J Cancer 23(16):3706–3712

    CAS  Google Scholar 

  332. D’Hondt V et al (2005) Will the dark sky over advanced renal cell carcinoma soon become brighter? Eur J Cancer 41(9):1246–1253

    PubMed  Google Scholar 

  333. Escudier B et al (2005) Randomized phase III trial of the Raf kinase and VEGFR inhibitor sorafenib (BAY 43–9006) in patients with advanced renal cell carcinoma (RCC). J Clin Oncol 23(16_suppl):4510–4510

    Google Scholar 

  334. Eelen G et al (2020) Basic and therapeutic aspects of angiogenesis updated. Circ Res 127(2):310–329

    CAS  PubMed  Google Scholar 

  335. De Palma M, Biziato D, Petrova TV (2017) Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer 17(8):457–474

    PubMed  Google Scholar 

  336. Mansoori B et al (2017) The different mechanisms of cancer drug resistance: a brief review. Adv Pharm Bull 7(3):339

    CAS  PubMed  PubMed Central  Google Scholar 

  337. Liu CH et al (2017) Animal models of ocular angiogenesis: from development to pathologies. FASEB J 31(11):4665–4681

    CAS  PubMed  PubMed Central  Google Scholar 

  338. Kleinman HK, Martin, GR (2005) Matrigel: basement membrane matrix with biological activity. In: Seminars in cancer biology. Elsevier, Amsterdam

Download references

Acknowledgements

Part of the research reported in this paper was supported by National Institute of Dental & Craniofacial Research of the National Institutes of Health under award numbers R15DE027533, 1 R56DE029191-01A1 and 3R15DE027533-01A1W1. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Chemistry, National Cheng Kung University, Tainan, 701, Taiwan

    Mohsen Akbarian

  2. Division of Biomaterials and Biomechanics, Department of Restorative Dentistry, School of Dentistry, Oregon Health and Science University, Portland, OR, USA

    Luiz E. Bertassoni

  3. Marquette University School of Dentistry, Milwaukee, WI, 53233, USA

    Lobat Tayebi

Authors
  1. Mohsen Akbarian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luiz E. Bertassoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lobat Tayebi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors have contributed equally.

Corresponding author

Correspondence to Lobat Tayebi.

Ethics declarations

Conflict of interest

There are no conflicts to declare.

Ethics approval and consent to participate

Not applicable.

Consent for publication

The authors give their consents for the publication of contents of this paper to be published in the Cellular and Molecular Life Sciences.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akbarian, M., Bertassoni, L.E. & Tayebi, L. Biological aspects in controlling angiogenesis: current progress. Cell. Mol. Life Sci. 79, 349 (2022). https://doi.org/10.1007/s00018-022-04348-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00018-022-04348-5

Keywords

Search

Navigation