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Jagged Mediates Differences in Normal and Tumor Angiogenesis by Affecting Tip-Stalk Fate Decision

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Jagged Mediates Differences in Normal and Tumor Angiogenesis by Affecting Tip-Stalk Fate Decision Jagged mediates differences in normal and tumor angiogenesis by affecting tip-stalk fate decision Marcelo Boaretoa,b, Mohit Kumar Jollya,c, Eshel Ben-Jacoba,d,1, and José N. Onuchica,2 aCenter for Theoretical Biological Physics, Rice University, Houston, TX 77005; bInstitute of Physics, University of Sao Paulo, Sao Paulo 05508, Brazil; cDepartment of Bioengineering, Rice University, Houston, TX 77005; and dSchool of Physics and Astronomy, Tel Aviv University, Tel Aviv 69978, Israel Contributed by José N. Onuchic, June 19, 2015 (sent for review April 30, 2015) Angiogenesis is critical during development, wound repair, and (5, 6) (Fig. 1A). Therefore, Notch-Delta signaling between two cancer progression. During angiogenesis, some endothelial cells interacting cells forms an intercellular double negative feedback adopt a tip phenotype to lead the formation of new branching loop, and the two cells tend to adopt different fates: one cell be- vessels; the trailing stalk cells proliferate to develop the vessel. Notch haves as a sender [high ligand (Delta), low receptor (Notch)] and and VEGF signaling mediate the selection of these tip endothelial the other one behaves as a receiver [low ligand (Delta), high re- cells. However, how Jagged, a Notch ligand that is overexpressed in ceptor (Notch)]. This process of lateral inhibition has a crucial role cancer, affects angiogenesis remains elusive. Here, by developing a in generating a checkerboard-like or “salt-and-pepper” pattern, as theoretical framework for Notch-Delta-Jagged-VEGF signaling, we observed during bristle patterning in flies and inner ear patterning found that higher production levels of Jagged destabilizes the tip in vertebrates (7). Conversely, Notch-Jagged signaling generates and stalk cell fates and can give rise to a hybrid tip/stalk phenotype an intercellular double positive feedback loop, enabling the two that leads to poorly perfused and chaotic angiogenesis, which is a interacting cells to adopt similar fates: a hybrid sender/receiver [high hallmark of cancer. Consistently, the signaling interactions that ligand (Jagged), high receptor (Notch)] fate. This process of lateral cis- restrict Notch-Jagged signaling, such as Fringe, inhibition, and in- induction is crucial during sensing development and the formation creased production of Delta, stabilize tip and stalk fates and limit the of a smooth muscle wall around a nascent artery (6, 8). existence of hybrid tip/stalk phenotype. Our results underline how Besides asymmetric modulation by NICD, N-D and N-J sig- overexpression of Jagged can transform physiological angiogenesis naling can also be differentially regulated by glycosyltransferase into pathological one. Fringe. Fringe modifies Notch such that the modified (or gly- cosylated) Notch has a higher chance to bind to Delta, but a angiogenesis | Notch signaling | Jagged | VEGF signaling | lower chance to bind to Jagged (9). Importantly, Fringe, can also tumor angiogenesis be activated by NICD in some biological contexts (10). These different dynamics of Notch-Delta and Notch-Jagged sig- ngiogenesis, the formation of new blood vessels from existing naling allow them to play complementary roles during angiogenesis. Aones, is a vital process during embryonic development, ho- Notch-Delta signaling plays a crucial role in selecting the tip cell in meostasis, and tumor progression (1). This process starts when cells response to VEGF (11). The binding of VEGF-A (the key ligand of release angiogenic growth factors such as VEGF in response to VEGF family that responds to hypoxia) to VEGF receptor 2 hypoxia (lack of oxygen). These growth factors induce the forma- (VEGFR2) (the main mediator of VEGF-A signaling during an- tion of a new sprout, and the endothelial cell at the very front of “ ” giogenesis) up-regulates the production of Delta (DLL4) (12). this angiogenic sprout is called a tip cell. The tip cell extends DLL4 binds to Notch receptor on the neighboring cell and activates numerous filopodia toward the source of these growth factors and Notch signaling (NICD) in it. NICD inhibits VEGFR2, therefore migrates toward the direction of the upward gradient of the growth factor concentration, thereby leading a new angiogenic branch. The cells that follow the tip cell do not adopt a tip phenotype, but Significance rather form the stalk of the branch and proliferate to form the vessel lumen (2). A well-regulated balance between the migration Developing effective antiangiogenesis strategies remains clini- of tip cells and proliferation of stalk cells is essential for adequately cally challenging. Unlike physiological angiogenesis, pathological shaped nascent sprouts (3). angiogenesis comprises of many microvessels that do not fully The selection of the tip and the stalk cell fate is critical for de- mature or develop functionally, because the cell fate decision veloping a functional vessel. This decision is mediated by Notch about which endothelial cells become the tip and lead the fol- signaling pathway (2), an evolutionarily conserved cell–cell com- lowing stalk cells is dysregulated. We devised a specific theoret- munication pathway involved in cell fate decisions in multiple ical framework to decipher the cross-talk between two crucial contexts. This pathway is activated when Notch (transmembrane players of the decision-making process of tip and stalk cell fate: receptor) belonging to a particular cell interacts with Delta or VEGF and Notch-Delta-Jagged signaling. We find that high ex- Jagged (transmembrane ligands) belonging to its neighboring cell pression of Jagged, but not Delta, can destabilize the terminal (trans-activation), thereby releasing the Notch intracellular domain differentiation into tip or stalk cells and give rise to a hybrid tip/ (NICD). NICD then enters the nucleus and modulates the ex- stalk phenotype, a phenotype that can transform physiological into pathological angiogenesis. Our results offer insights into pression of many target genes of the Notch pathway, including both why tumor-stroma communication often implicates Jagged. the ligands Delta and Jagged. However, when Notch of a cell in- teracts with Delta or Jagged belonging to the same cell, no NICD is Author contributions: M.B., M.K.J., E.B.-J., and J.N.O. designed research; M.B. and M.K.J. produced; rather, both the receptor (Notch) and ligand (Delta or performed research; M.B., M.K.J., E.B.-J., and J.N.O. analyzed data; and M.B., M.K.J., Jagged) are degraded (cis-inhibition) and therefore the signaling is E.B.-J., and J.N.O. wrote the paper. not activated (4). The authors declare no conflict of interest. Despite generating the same signal (NICD), Notch signaling Freely available online through the PNAS open access option. activated via Delta and that via Jagged, or in other words, Notch- 1Deceased June 5, 2015. Delta (N-D) signaling and Notch-Jagged (N-J) signaling, have dif- 2To whom correspondence should be addressed. Email: [email protected]. ferent dynamics, because NICD asymmetrically modulates the ex- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. pression of the two ligands: it represses Delta but activates Jagged 1073/pnas.1511814112/-/DCSupplemental. E3836–E3844 | PNAS | Published online July 7, 2015 www.pnas.org/cgi/doi/10.1073/pnas.1511814112 Downloaded by guest on October 1, 2021 AB PNAS PLUS Fig. 1. Overview of the intracellular and intercellular interplay between Notch and VEGF signaling pathways. (A) Notch signaling is activated when the transmembrane receptor of one cell (Notch) binds to the transmembrane ligand (Delta or Jagged) of the neighboring cell (trans-activation). This trans- activation cleaves Notch to produce Notch Intracellular Domain (NICD) that is released in the cytoplasm and then enters the nucleus to modulate the tran- scription of many target genes. NICD can activate Notch and Jagged and inhibit Delta and VEGF receptor 2 (VEGFR2). Glycosylation of Notch by Fringe modifies Notch to have a higher affinity for binding to Delta and a lower affinity for binding to Jagged. Interaction between Notch receptor and ligands (Delta or Jagged) of the same cell (cis-inhibition) leads to the degradation of both the receptor and the ligand; thus, no NICD is generated. VEGF-A binds to VEGFR2, thus activating VEGF signaling in the cell that activates Delta (DLL4). (B) Cells with high levels of Delta, VEGFR2, and active VEGF signaling develop filopodia and migrate toward the VEGF-A gradient, leading the formation of the new branch and are called tip cells. DLL4 from tip cells inhibits the neighboring cells to also adopt a tip phenotype, thereby forcing them to adopt the stalk fate (low Dll4, high Jagged1, and NICD). Stalk cells, by virtue of the lateral induction characteristics of Notch-Jagged signaling, can induce neighboring cells to adopt a stalk cell, therefore elongating the lumen. making the adjacent cell less sensitive to the VEGF-A signal (12). lateral inhibition and can be critical for the emergence of a chaotic The cell with high Delta (and low NICD) becomes the tip, and the blood vessel network as seen during tumor angiogenesis. Finally, adjacent ones with low levels of Delta (and high NICD) become the we evaluate the role of both Fringe and cis-inhibition in the tip- stalk (12). This interplay between Notch and VEGF pathways is stalk cell fate decision. quite tight and dose dependent, i.e., many neighboring cells dy- namically compete to adopt the tip position but only one of them Results wins (13). However, unlike other contexts where Notch-Delta The Theoretical Framework. To explore the effects of Jagged in cell (N-D) signaling leads to salt-and-pepper patterns, i.e., pattern of fate determination during angiogenesis, we generalized our earlier alternate fates with a wavelength of one cell, in angiogenesis, the theoretical framework of Notch-Delta-Jagged signaling (15) to two tip cells are usually separated by a few stalk cells, all of which incorporate VEGF signaling. The equations that describe the dy- have low Delta but high Jagged (Jag1) levels (14).
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