Skip to main content
SpringerLink
Log in

The modes of angiogenesis: an updated perspective

  • Letter
  • Published:
Angiogenesis Aims and scope Submit manuscript

Abstract

Following the process of vasculogenesis during development, angiogenesis generates new vascular structures through a variety of different mechanisms or modes. These different modes of angiogenesis involve, for example, increasing microvasculature density by sprouting of endothelial cells, splitting of vessels to increase vascular surface area by intussusceptive angiogenesis, fusion of capillaries to increase blood flow by coalescent angiogenesis, and the recruitment of non-endothelial cells by vasculogenic mimicry. The recent reporting on coalescent angiogenesis as a new mode of vessel formation warrants a brief overview of angiogenesis mechanisms to provide a more complete picture. The journal Angiogenesis is devoted to the delineation of the different modes and mechanisms that collectively dictate blood vessel formation, inhibition, and function in health and disease.

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

The figure was created with BioRender.com and is available on request

References

  1. Nitzsche B, Rong WW, Goede A, Hoffmann B, Scarpa F, Kuebler WM, Secomb TW, Pries AR (2021) Coalescent angiogenesis-evidence for a novel concept of vascular network maturation. Angiogenesis 25(1):35

    Article  PubMed  PubMed Central  Google Scholar 

  2. Pezzella F, Kerbel RS (2022) On coalescent angiogenesis and the remarkable flexibility of blood vessels. Angiogenesis 25(1):1–3

    Article  PubMed  Google Scholar 

  3. Dudley AC, Griffioen AW (2023) Pathological angiogenesis: mechanisms and therapeutic strategies. Angiogenesis. https://doi.org/10.1007/s10456-023-09876-7

    Article  PubMed  PubMed Central  Google Scholar 

  4. Lin Y, Banno K, Gil CH, Myslinski J, Hato T, Shelley WC, Gao H, Xuei X, Liu Y, Basile D et al (2023) Origin, prospective identification, and function of circulating endothelial colony forming cells in mouse and man. JCI Insight. https://doi.org/10.1172/jci.insight.164781

    Article  PubMed  PubMed Central  Google Scholar 

  5. Dight J, Zhao J, Styke C, Khosrotehrani K, Patel J (2022) Resident vascular endothelial progenitor definition and function: the age of reckoning. Angiogenesis 25(1):15–33

    Article  CAS  PubMed  Google Scholar 

  6. Hillen F, Griffioen AW (2007) Tumor vascularization; sprouting angiogenesis and beyond. Cancer Met Rev 26(3–4):13

    Google Scholar 

  7. Djonov V, Schmid M, Tschanz SA, Burri PH (2000) Intussusceptive angiogenesis: its role in embryonic vascular network formation. Circ Res 86(3):286–292

    Article  CAS  PubMed  Google Scholar 

  8. Djonov VG, Kurz H, Burri PH (2002) Optimality in the developing vascular system: branching remodeling by means of intussusception as an efficient adaptation mechanism. Dev Dyn 224(4):391–402

    Article  PubMed  Google Scholar 

  9. Zhang Y, Wang S, Dudley AC (2020) Models and molecular mechanisms of blood vessel co-option by cancer cells. Angiogenesis 23(1):17–25

    Article  PubMed  Google Scholar 

  10. Hu J, Bianchi F, Ferguson M, Cesario A, Margaritora S, Granone P, Goldstraw P, Tetlow M, Ratcliffe C, Nicholson AG et al (2005) Gene expression signature for angiogenic and nonangiogenic non-small-cell lung cancer. Oncogene 24(7):1212–1219

    Article  CAS  PubMed  Google Scholar 

  11. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe’er J, Trent JM, Meltzer PS, Hendrix MJ (1999) Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 155(3):739–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Li A, Zhu L, Lei N, Wan J, Duan X, Liu S, Cheng Y, Wang M, Gu Z, Zhang H et al (2022) S100A4-dependent glycolysis promotes lymphatic vessel sprouting in tumor. Angiogenesis 26(1):19

    Article  PubMed  Google Scholar 

  13. Chen XJ, Wei WF, Wang ZC, Wang N, Guo CH, Zhou CF, Liang LJ, Wu S, Liang L, Wang W (2021) A novel lymphatic pattern promotes metastasis of cervical cancer in a hypoxic tumour-associated macrophage-dependent manner. Angiogenesis 24(3):549–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Fankhauser M, Broggi MAS, Potin L, Bordry N, Jeanbart L, Lund AW, Da Costa E, Hauert S, Rincon-Restrepo M, Tremblay C et al (2017) Tumor lymphangiogenesis promotes T cell infiltration and potentiates immunotherapy in melanoma. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aal4712

    Article  PubMed  Google Scholar 

  15. Blanchard L, Girard JP (2021) High endothelial venules (HEVs) in immunity, inflammation and cancer. Angiogenesis 24(4):719–753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Smadja DM, Mentzer SJ, Fontenay M, Laffan MA, Ackermann M, Helms J, Jonigk D, Chocron R, Pier GB, Gendron N et al (2021) COVID-19 is a systemic vascular hemopathy: insight for mechanistic and clinical aspects. Angiogenesis 24(4):755–788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ackermann M, Mentzer SJ, Jonigk D (2020) Pulmonary Vascular Pathology in Covid-19. Reply. N Engl J Med 383(9):888–889

    PubMed  Google Scholar 

  18. Smadja DM, Guerin CL, Chocron R, Yatim N, Boussier J, Gendron N, Khider L, Hadjadj J, Goudot G, Debuc B et al (2020) Angiopoietin-2 as a marker of endothelial activation is a good predictor factor for intensive care unit admission of COVID-19 patients. Angiogenesis 23(4):611–620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Philippe A, Chocron R, Gendron N, Bory O, Beauvais A, Peron N, Khider L, Guerin CL, Goudot G, Levasseur F et al (2021) Circulating Von Willebrand factor and high molecular weight multimers as markers of endothelial injury predict COVID-19 in-hospital mortality. Angiogenesis 24(3):505–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Philippe A, Gendron N, Bory O, Beauvais A, Mirault T, Planquette B, Sanchez O, Diehl JL, Chocron R, Smadja DM (2021) Von Willebrand factor collagen-binding capacity predicts in-hospital mortality in COVID-19 patients: insight from VWF/ADAMTS13 ratio imbalance. Angiogenesis 24(3):407–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bhogal P, Paul G, Collins G, Jaffer O (2021) Letter in response to: circulating von Willebrand factor and high molecular weight multimers as markers of endothelial injury predict COVID-19 in-hospital mortality. Angiogenesis 24(3):413–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Rovas A, Buscher K, Osiaevi I, Drost CC, Sackarnd J, Tepasse PR, Fobker M, Kuhn J, Braune S, Gobel U et al (2022) Microvascular and proteomic signatures overlap in COVID-19 and bacterial sepsis: the MICROCODE study. Angiogenesis 25(4):503–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Klouda T, Hao Y, Kim H, Kim J, Olejnik J, Hume AJ, Ayyappan S, Hong X, Melero-Martin J, Fang Y et al (2022) Interferon-alpha or -beta facilitates SARS-CoV-2 pulmonary vascular infection by inducing ACE2. Angiogenesis 25(2):225–240

    Article  CAS  PubMed  Google Scholar 

  24. Osiaevi I, Schulze A, Evers G, Harmening K, Vink H, Kumpers P, Mohr M, Rovas A (2022) Persistent capillary rarefication in long COVID syndrome. Angiogenesis 26(1):8

    Google Scholar 

  25. Riera-Mestre A, Iriarte A, Moreno M, Del Castillo R, Lopez-Wolf D (2021) Angiogenesis, hereditary hemorrhagic telangiectasia and COVID-19. Angiogenesis 24(1):13–15

    Article  CAS  PubMed  Google Scholar 

  26. Werlein C, Ackermann M, Stark H, Shah HR, Tzankov A, Haslbauer JD, von Stillfried S, Bulow RD, El-Armouche A, Kuenzel S et al (2023) Inflammation and vascular remodeling in COVID-19 hearts. Angiogenesis 26(2):233–248

    Article  CAS  PubMed  Google Scholar 

  27. Henry BM, de Oliveira MHS, Cheruiyot I, Benoit JL, Cooper DS, Lippi G, Le Cras TD, Benoit SW (2021) Circulating level of Angiopoietin-2 is associated with acute kidney injury in coronavirus disease 2019 (COVID-19). Angiogenesis 24(3):403–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Rovas A, Osiaevi I, Buscher K, Sackarnd J, Tepasse PR, Fobker M, Kuhn J, Braune S, Gobel U, Tholking G et al (2021) Microvascular dysfunction in COVID-19: the MYSTIC study. Angiogenesis 24(1):145–157

    Article  CAS  PubMed  Google Scholar 

  29. Pasut A, Becker LM, Cuypers A, Carmeliet P (2021) Endothelial cell plasticity at the single-cell level. Angiogenesis 24(2):311–326

    Article  PubMed  PubMed Central  Google Scholar 

  30. Koch PS, Lee KH, Goerdt S, Augustin HG (2021) Angiodiversity and organotypic functions of sinusoidal endothelial cells. Angiogenesis 24(2):289–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Marziano C, Genet G, Hirschi KK (2021) Vascular endothelial cell specification in health and disease. Angiogenesis 24(2):213–236

    Article  PubMed  PubMed Central  Google Scholar 

  32. Margadant C (2021) Endothelial heterogeneity and plasticity. Angiogenesis 24(2):197–198

    Article  PubMed  Google Scholar 

  33. Jafree DJ, Long DA, Scambler PJ, Ruhrberg C (2021) Mechanisms and cell lineages in lymphatic vascular development. Angiogenesis 24(2):271–288

    Article  PubMed  PubMed Central  Google Scholar 

  34. Mauri C, van Impel A, Mackay EW, Schulte-Merker S (2021) The adaptor protein Grb2b is an essential modulator for lympho-venous sprout formation in the zebrafish trunk. Angiogenesis 24(2):345–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ruter DL, Liu Z, Ngo KM, Marvin XS, Buglak A, Kidder DB, Bautch EJ (2021) SMAD6 transduces endothelial cell flow responses required for blood vessel homeostasis. Angiogenesis 24(2):387–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Canu G, Ruhrberg C (2021) First blood: the endothelial origins of hematopoietic progenitors. Angiogenesis 24(2):199–211

    Article  PubMed  PubMed Central  Google Scholar 

  37. Hong X, Oh N, Wang K, Neumeyer J, Lee CN, Lin RZ, Piekarski B, Emani S, Greene AK, Friehs I et al (2021) Human endothelial colony-forming cells provide trophic support for pluripotent stem cell-derived cardiomyocytes via distinctively high expression of neuregulin-1. Angiogenesis 24(2):327–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tang X, Wang JJ, Wang J, Abboud HE, Chen Y, Zhang SX (2021) Endothelium-specific deletion of Nox4 delays retinal vascular development and mitigates pathological angiogenesis. Angiogenesis 24(2):363–377

    Article  CAS  PubMed  Google Scholar 

  39. Corvera S, Solivan-Rivera J, Yang Loureiro Z (2022) Angiogenesis in adipose tissue and obesity. Angiogenesis 25(4):439–453

    Article  PubMed  PubMed Central  Google Scholar 

  40. Sun D, Wang J, Toan S, Muid D, Li R, Chang X, Zhou H (2022) Molecular mechanisms of coronary microvascular endothelial dysfunction in diabetes mellitus: focus on mitochondrial quality surveillance. Angiogenesis 25(3):307–329

    Article  PubMed  Google Scholar 

  41. Griffioen AW, Dudley AC (2021) Angiogenesis: a year in review. Angiogenesis 24(2):195–196

    Article  PubMed  PubMed Central  Google Scholar 

  42. Griffioen AW, Dudley AC (2022) The rising impact of angiogenesis research. Angiogenesis 25(4):435–437

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Immunology, and Cancer Biology, The University of Virginia, & The UVA Comprehensive Cancer Center, Charlottesville, VA, 22908, USA

    Andrew C. Dudley

  2. Angiogenesis Laboratory, Department of Medical Oncology, Amsterdam University Medical Center, Vrije Universiteit Amsterdam, Cancer Center Amsterdam, Amsterdam, The Netherlands

    Arjan W. Griffioen

Authors
  1. Andrew C. Dudley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arjan W. Griffioen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ACD and AWG wrote the manuscript text.

Corresponding authors

Correspondence to Andrew C. Dudley or Arjan W. Griffioen.

Ethics declarations

Competing interests

The authors declare no competing interests.

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

Dudley, A.C., Griffioen, A.W. The modes of angiogenesis: an updated perspective. Angiogenesis 26, 477–480 (2023). https://doi.org/10.1007/s10456-023-09895-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10456-023-09895-4

Search

Navigation