Adipocyte-Endothelial Cell Crosstalk in Angiolipoma: Contribution of the Extracellular Galectin-1, -3 and -8 and their Binding Partners

Main Article Content

Enrique Arciniegas Andrés Duque Héctor Rojas Jacinto Pineda Antonio Salgado Alejandra Urbano Ana María Sáenz Richard Ramírez

Abstract

Angiolipomas are benign subcutaneous nodules composed of mature adipose tissue with thin-walled, dilated and tortuous small blood vessels, displaying intraluminal deposition of fibrin microthrombi formed from fibrinogen. The latter, considered not only as a diagnostic hallmark of angiolipoma, but also as a marker of vascular permeability. It is known that human adipose tissue (AT) growth, expansion, and maintenance is angiogenesis dependent and involves adipocytes, immune cells , fibroblasts, adipose stem cells and preadipocytes, all of them supported by an extracellular matrix. Interestingly, emerging evidence have emphasized that adipocytes maintain a bidirectional communication (crosstalk) with adipose endothelial cells (ECs) in healthy and pathological tissues and that this reciprocal and dynamic communication is crucial not only for the growth, expansion and maintenance of the AT, but also for the formation of new capillaries (angiogenesis) or microvasculature remodeling. However, the signals and mediators involved in this communication remain to be investigated.


Herein, we show that in angiolipoma GAL-1, -3 and -8 and some of their binding partners that includes proteoglycans such as perlecan, agrin, CD44 and endocan, as well as glycoproteins including TLR4, fibronectin, thrombospondin-1, integrin β1, PECAM-1, endoglin, VE-cadherin, and neuropilin-1, were immunolocalized around mature adipocytes that were in close proximity to small blood vessels, as well as in the ECs lining the lumen of these vessels.


We propose that in angiolipoma, GAL-1, -3 and -8 acting in concert with their binding partners form a supramolecular multivalent structure on the surface of mature adipocytes and ECs that might be facilitating the bidirectional communication (crosstalk) between adipocytes and ECs, contributing to the mature adipocytic expansion and the new vasculature formation (angiogenesis) or microvasculature remodeling.

Keywords: Angiolipoma, adipocyte, endothelial cell, crosstalk, galectins, Gal-glycan lattice

Article Details

How to Cite
ARCINIEGAS, Enrique et al. Adipocyte-Endothelial Cell Crosstalk in Angiolipoma: Contribution of the Extracellular Galectin-1, -3 and -8 and their Binding Partners. Medical Research Archives, [S.l.], v. 14, n. 3, mar. 2026. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/7267>. Date accessed: 06 apr. 2026. doi: https://doi.org/10.18103/mra.v14i3.7267.
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Research Articles

References

1. Alonso S, Rodríguez-Peralto JL, Pérez-Espejo G. Metastasis of cutaneous malignant melanoma to angiolipoma: the tumor-to-tumor metastasis phenomenon. J Cutan Pathol. 2003; 30(5):323-325.
2. Lapidoth M, Ben Amitai D, Feinmesser M, Akerman L. Capillary malformation associated with angiolipoma: analysis of 127 consecutive clinic patients. Am J Clin Dermatol. 2008; 9(6):389-392.
3. Heng W, Lu L, Wang J. Cellular angiolipoma: a clinicopathological and immunohistochemical study of 12 cases. Am J Dermatopathol. 2013; 35(2):220-225.
4. Saggini A, Santonja C, Nájera L, Palmedo G, Kutzner H. Frequent activating PIK3CA mutations in sporadic angiolipoma. J Cutan Pathol. 2021; 48(2):211-216.
5. Díaz-Flores L, Gutiérrez R, Pino García M et al. Intussusceptive angiogenesis facilitated by microthrombosis has an important example in angiolipoma. An ultrastructural and immunohistochemical study. Histol Histopathol. 2023; 38(1):29-46.
6. Kransdorf MJ, Larsen BT, Goulding, KA, Cumsky JL, Hwang S, Long J. Angiolipoma: a review of 778 lesions in 344 patients. Skeletal Radiol. 2023; 52(3):541-552.
7. Arciniegas E, Rojas H, Pineda J, et al. Endothelial TLR4 Activation by endogenous ligands contributes to small blood vessels formation in angiolipoma. J Dermatol Res. 2024; 5(3):1-16. doi.org/10.46889/JDR.2024.5311.
8. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol. 1999; 237:97–132.
9. Wu M-H, Ying N-W, Hong T-M, Chiang W-F, Lin Y-T, Chen Y-L. Galectin-1 induces vascular permeability through the neuropilin-1/vascular endothelial growth factor receptor-1 complex. Angiogenesis. 2014. doi.org/10.1007/s10456-014-9431-8.
10. Rupnick MA, Panigrahy D, Zhang Ch-Y, et al. Adipose tissue mass can be regulated through the vasculature. PNAS. 2002; 99(16);10730-10735.
11. Hausman GJ, Richardson RL. Adipose tissue angiogenesis. J. Anim. Sci. 2004; 82:925–934.
12. Alvarez-Llamas G, Szalowska E, de Vries MP, Weening D, Landman K, Hoek A. Characterization of the human visceral adipose tissue secretome. Mol Cell Proteomics. 2007; 6(4):589-600.
13. Cao Y. Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases. Nat Rev Drugs Discov. 2010; 9:107-115.
14. Christiaens V, Lijnen HR. Angiogenesis and development of adipose tissue. Mol Cell Endocrinol. 2010; 318:2–9.
15. Crewe C, An YA, Scherer PE. The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. J Clin Invest. 2017; 127(1):74-82.
16. Ruiz-Ojeda FJ, Méndez-Gutiérrez A, Aguilera MC, Plaza-Díaz J. Extracellular matrix remodeling of adipose tissue in obesity and metabolic diseases. Int J Mol Sci. 2019, 20, 4888. doi.org/10.3390/ijms20194888.
17. Herold J, Kalucka J. Angiogenesis in adipose tissue: The interplay between adipose and endothelial cells. Front Physiol. 2021; 11;624903. doi.org/10.3389/fphys.2020.624903.
18. Sun K, Li X, Scherer PE. Extracellular matrix (ECM) and fibrosis in adipose tissue: overview and perspectives. Compr Physiol. 2023; 13(1):4387–4407. doi.org/10.1002/cphy.c220020.
19. Corvera S. Cellular Heterogeneity in Adipose Tissues. Annu Rev Physiol. 2021; 10; 83:257–278.
20. Corvera S, Solivan‑Rivera J, Loureiro ZY. Angiogenesis in adipose tissue and obesity. Angiogenesis. 2022; 25:439–453.
21. Maniyadath B, Zhang Q, Gupta RK. Mandrup S. Adipose tissue at single cell resolution. Cell Metab. 2023; 35(3):386–413.
22. Santillana N, Astudillo-Guerrero C, D’Espessailles A, Cruz G. White adipose tissue dysfunction: pathophysiology and emergent measurements. Nutrients. 2023; 15, 1722.
23. Auger Ch, Kajimura S. Adipose tissue remodeling in pathophysiology. Annu Rev Pathol. 2023; 18: 71–93.
24. Johnston EK, Abbott RD. Adipose tissue development relies on coordinated extracellular matrix remodeling, angiogenesis, and adipogenesis. Biomedicines. 2022; 10, 2227. doi.org/10.3390/biomedicines10092227
25. Iacobini C, Vitale M, Haxhi J, Menini S, Pugliese G. Impaired remodeling of white adipose tissue in obesity and aging: from defective adipogenesis to adipose organ dysfunction. Cells. 2024; 13, 763. doi.org/10.3390/cells13090763.
26. Arderiu G, Civit-Urgell A, Díez-Caballero A , Moscatiello F, Ballesta C, Badimon L. Differentiation of adipose tissue mesenchymal stem cells into endothelial cells depends on fat depot conditions: regulation by miRNA. Cells. 2024; 13, 513. doi.org/10.3390/cells13060513.
27. Mo Y-Y, Han Y-X, Xu S-N, et al. Adipose tissue plasticity: a comprehensive definition and multidimensional insight. Biomolecules. 2024; 14, 1223. doi.org/10.3390/biom14101223.
28. Chaurasiya V, Nidhina Haridas PA, Olkkonen VM. Adipocyte-endothelial cell interplay in adipose tissue physiology. Biochem Pharmacol. 2024; 222, 116081. doi.org/10.1016/j.bcp.2024.116081.
29. Aoki S, Toda S, Sakemi T, Sugihara H. Coculture of endothelial cells and mature adipocytes actively promotes immature preadipocyte development in vitro. Cell Struct Function. 2003; 28:55-60.
30. Rojas-Rodriguez R, Gealekman O, Kruse ME, et al. Adipose tissue angiogenesis assay. Methods Enzymol. 2014; 537: 75–91.
31. Blázquez Medela AM, Penton A, Bostrom KI, Saparov A, Jumabay M. Generation of Vascular Networks from Adipocytes in vitro. Int J Cell Sci Mol Biol. 2019; 6(2):1-12.
32. Sabaratnam R, Svenningsen P. Adipocyte- endothelium crosstalk in obesity. Front Endocrinol. 2021; 12;681290. doi.org/10,3389/fendo.2021,681290.
33. Hammel JH, Bellas E. Endothelial cell crosstalk improves browning but hinders white adipocyte maturation in 3D engineered adipose tissue. Integr Biol. 2020; 12, 81–89. doi.org/10.1093/intbio/zyaa006.
34. Liao Z-Z, Ran L, Qi X-H, et al. Adipose endothelial cells mastering adipose tissues metabolic fate. ADIPOCYTE. 2022; 11(1):108–119.
35. Sorrell JM, Caplan AI. Heparan sulfate: a regulator of white adipocyte differentiation and of vascular/adipocyte interactions. Biomedicines. 2022; 10, 2115. doi.org/10.3390/biomedicines10092115.
36. Chaurasiya V, Pham DD, Harju J, et al. Human visceral adipose tissue microvascular endothelial cell isolation and establishment of co-culture with White adipocytes to analyze cell-cell communication. Exp Cell Res. 2023; 113819. doi.org/10.106/JYEXCR,2023.113819.
37. Vezza T, Vıctor VM. Bridging the gap: how endothelial-adipocyte Cx43 mediated gap junctions could revolutionize adiposity regulation. FUNCTION. 2024; 5(6): zqae046. doi.org/10.1093/function/zqae046.
38. Asterholma IWA, Kusminskia ChM, Buenoa AC, et al. Dichotomous effects of VEGF-A on adipose tissue dysfunction. PNAS. 2012; 109(15):5874-5879.
39. Dudley AC, Griffioen AW. Pathological angiogenesis: mechanisms and therapeutic strategies. Angiogenesis. 2023; 26:313–347.
40. Zhang SM, L Zuo L, Zhou Q, et al. Expression and distribution of endocan in human tissues. Biotechnic Histochem. Early Online, 2011;1–7. doi.org/10.3109/10520295.2011.577754.
41. Delehedde M, Devenyns L, Maurage C-A, Vivès RR. Endocan in cancers: a lesson from a circulating dermatan sulfate proteoglycan. Int J Cell Biol. 2013 https://dx.doi.org/10.1155/2013/705027.
42. Klisic A, Patoulias D. The role of endocan in cardiometabolic disorders. Metabolites. 2023; 13, 640. doi.org/10.3390/metabo13050640.
43. Grote K, Schütt H, Schieffer B. Toll-like receptors in angiogenesis. Scientific World Journal. 2011; 11:981-91.
44. Ren M, Li R, Luo M, et al. Endothelial cells but not platelets are the major source of Toll-like receptor 4 in the arterial thrombosis and tissue factor expression in mice. Am J Physiol Regul Integr Comp Physiol. 2014; 307(7):R901-7.
45. Salvador B, Arranz A, Francisco S, et al. Modulation of endothelial function by Toll like receptors. Pharmacol Res. 2016; 108:46-56.
46. Wang Y, Song E, Bai B, Vanhoutte PM. Toll-like receptors mediating vascular malfunction: Lessons from receptor subtypes. Pharmacol Ther. 2016; 158:91-100.
47. Bhagwani A, Thompson AAR, Farkas L. When innate immunity meets angiogenesis-the role of Toll-like receptors in endothelial cells and pulmonary hypertension. Front Med. 2020; 7:352. doi.org/10.3389/fmed.2020.00352.
48. Stierschneider A, Wiesner C. Shedding light on the molecular and regulatory mechanisms of TLR4 signaling in endothelial cells under physiological and inflamed conditions. Front Immunol. 2023; 14:1264889. doi.org/10.3389/fimmu.2023.1264889.
49. Bès-Houtmann S, Roche R, Hoareau L, et al. Presence of functional TLR2 and TLR4 on human adipocytes. Histochem Cell Biol. 2007; 127:131–137.
50. Vaure C, Liu Y. A comparative review of Toll-Like Receptor 4 expression and functionality in different animal species. Front Immu. 2014 doi.org/10.3389/fimmu.2014.00316.
51. Frey H, Schroeder N, Manon-Jensen T, Iozzo RV, Schaefer L. Biological interplay between proteoglycans and their innate immune receptors in inflammation. FEBS J. 2013; 280(10):2165–2179.
52. Pietsch J, Batra A, Stroh T, et al. Toll-like receptor expression and response to specific stimulation in adipocytes and preadipocytes: On the role of fat in inflammation. Ann N Y Acad Sci. 2006; 1072:407–409.
53. Konner AC, Bruning JC. Toll-like receptors: Linking inflammation to metabolism. Trends Endocrinol Metab. 2011; 22:16–23.
54. Cuesta N, Fernández-Veledo S, Punzón C, et al. Opposing actions of TLR2 and TLR4 in adipocyte differentiation and mature-onset obesity. Int J Mol Sci. 2022; 23, 15682. doi.org/10.3390/ijms232415682.
55. Barondes SH, Castronovo V, Cooper DN, et al. Galectins: a family of animal β-galactoside-binding lectins. Cell. 1994; 76: 597-598.
56. Yang RY, Rabinovich GA, Liu F-T. Galectins: structure, function and therapeutic potential. Expert Rev Mol Med. 2008 ; 10: e17.
57. Liu F_T, Rabinovich GA. Galectins: regulators of acute and chronic inflammation. Ann NY Acad Sci. 2010 ; 1183: 158-182.
58. Vasta GR. Galectins as pattern recognition receptors: structure,function, and evolution. Adv Exp Med Biol. 2012 ; 946: 21-36.
59. Thiemann S, Baum LG. Galectins and immune responses-just how do they do those things they do?. Annu Rev Immunol. 2016 ; 34: 243-264.
60. Cummings RD, Liu F-T, Rabinovich GA et al. Galectins. In: Varki A, Cummings RD, Esko JD, et al editors. Essentials of glycobiology (internet). Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2022. Chapter 36.
61. Troncoso MF, Elola MT, Blidner AG, Sarrias1 L, Espelt MV, Rabinovich GA. The universe of galectin-binding partners and their functions in health and disease. J Biol Chem. 2023; 299(12) 105400.
62. Nangia-Makker F, Honjo Y, Sarvis R, et al. Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am J Pathol. 2000; 156;3:899-909.
63. Brewer CF, Miceli MC, Baum LG. Clusters, bundles, arrays and lattices: novel mechanisms for lectin–saccharide-mediated cellular interactions. Curr Opin Struct Biol. 2002; 12:616–623.
64. Elola MT, Wolfenstein-Todel C, Troncoso, MF, Vastab GR, Rabinovich GA. Galectins: matricellular glycan-binding proteins linking cell adhesion, migration, and survival. Cell Mol Life Sci. 2007; 64;1679 – 1700.
65. Delgado V, Nugnes LG, Colombo LL, et al. Modulation of endothelial cell migration and angiogenesis: a novel function for the “tandem-repeat” lectin galectin-8. FASEB J. 2011; 25;242-254.
66. Troncoso MF, Ferragut F, Bacigalupo ML, Cárdenas Delgado VM, Nugnes LG, Gentilini L, et al. Galectin-8 a matricellular lectin with key roles in angiogenesis. Glycobiology. 2014; 24(10):907-914.
67. Compagno D, Jaworski FM, Gentilini L, et al. Galectins: major signaling modulators inside and outside the cell. Curr Mol Med. 2014 ; 14: 1-22.
68. Elola MT, Blidner AG, Ferragut F, Bracalente C, Rabinovich GA. Assembly, organization and regulation of cell-surface receptors by lectin-glycan complex. Biochem J. 2015 ; 469:1-16.
69. Thijssen VL. Galectins in endothelial cell biology and angiogenesis: the basics. Biomolecules. 2021; 11, 1386.
70. Arciniegas E, Carrillo LM, Rojas H, et al. Plump endothelial cells integrated into pre-existing venules contribute to the formation of mother and daughter vessels in pyogenic granuloma: possible role of Gal-1, -3 and -8. Scars Burn Heal. 2021 ; 7:1-12.
71. Thijssen VJL. Vascular galectins in tumor angiogenesis and cancer immunity. Seminars Immunopathol. 2024 ; 46:3. doi.org/10.1007/s00281-024-01014-9.
72. Garner OB, Baum LG. Galectin-glycan lattices regulate cell-surface glycoprotein organization and signaling. Biochem Soc Trans. 2008 ; 36:1472-1477.
73. Nabi IR, Shankar J, Demis JW. The galectin lattice at a glance. J Cell Sci. 2015 ; 128:2213-2219.
74. Arciniegas E, Carrillo LM, Rojas H, Ramírez R, Chopite M. Galectin-1 and galectin-3 and their potential binding partners in the dermal thickening of keloids. Am J Dermatopathol. 2019 ; 41:193-204.
75. Porębska N, Pozniak M, Matynia A, et al. Galectins as modulators of receptor tyrosine kinases signaling in health and disease. Cytokines Growth Factors Rev. 2021; 60:89-106.
76. Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. 2011; 3:a004952.
77. Iozzo, RV. Heparan sulfate proteoglycans: Intricate molecules with intriguing functions. J Clin Invest. 2001; 108:165–167.
78. Gallagher J. Fell-Muir Lecture: Heparan sulphate and the art of cell regulation: A polymer chain conducts the protein orchestra. Int J Exp Pathol. 2015; 96:203–231.
79. Park H, Kim M, Kim H-J, et al. Heparan sulfate proteoglycans (HSPGs) and chondroitin sulfate proteoglycans (CSPGs) functions endocytic receptors for an internalizing anti-nucleic acid antibody. Scientific Reports. 2017; 7:14373. doi:10.1038/s41598-017-14793-z.
80. Pankov R, Yamada KM. Fibronectin at a glance. J Cell Sci. 2002; 115:3861–3863.
81. Resovi A, Pinessi D, Chiorino G, Taraboletti G. Current understanding of the thrombospondin-1 interactome. Matrix Biol. 2014; 37:83–91.
82. Nakagawa H, Zheng M, Hakomori S-I, Tsukamoto Y, Kawamura Y, Takahashi N. Detailed oligosaccharide structures of human integrin α5β1 analyzed by a three-dimensional mapping technique. Eur J Biochem. 1996; 237:76-85.
83. Gu J, Taniguchi N. Regulation of integrin functions by N-Glycans. Glycoconjugate J. 2004; 21:9-15.
84. Rhodes, JM, Simons M. The extracellular matrix and blood vessel formation: Not just a scaffold. J. Cell Mol Med. 2007; 11:176–205.
85. Singh P, Carraher C, Schwarzbauer JE. Assembly of fibronectin extracellular matrix. Annu Rev Cell Dev Biol. 2010; 26:397–419.
86. Farnier C, Krief S, Blache M, et al. Adipocyte functions are modulated by cell size change: potential involvement of an integrin/ERK signalling pathway. Int J Obes Relat Metab Disord. 2003; 27(10):1178-1186.
87. Uetakia M, Onishia N, Okib Y, et al. Regulatory roles of fibronectin and integrin α5 in reorganization of the actin cytoskeleton and completion of adipogenesis. Mol Biol Cell. 2022; 78:1–11.
88. Sottile J. Regulation of angiogenesis by extracellular matrix. Biochim Biophys Acta (BBA)—Bioenerg. 2004; 1654:13–22.
89. Davis GE, Senger DR. Endothelial extracellular matrix: Biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res. 2005; 97:1093–1107.
90. Mongiat M, Andreuzzi E, Tarticchio G, Paulitti A. Extracellular matrix, a hard player in angiogenesis. Int J Mol Sci. 2016; 17, 1822. doi:10.3390/ijms17111822.
91. Kretschmer M, Rüdiger D, Zahler S. Mechanical aspects of angiogenesis. Cancers. 2021; 13, 4987. doi.org/10.3390/cancers13194987.
92. DeLisser HM, Christofidou-Solomidou M, Strieter RM, et al. Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol. 1997; 151:671-677.
93. Park S, DiMaio TA, Scheef EA, et al. PECAM-1 regulates proangiogenic properties of endothelial cells through modulation of cell-cell and cell-matrix interactions. Am J Physiol Cell Physiol. 2010; 299(6):C1468–C1484.
94. Privratsky JR, Paddock CM, Florey O, Newman DK, Muller WA, Newman PJ. Relative contribution of PECAM-1 adhesion and signaling to the maintenance of vascular integrity. J Cell Sci. 2011; 124:1477-1485.
95. Kitazume S, Imamaki R, Ogawa K, Taniguchi N. Sweet role of platelet endothelial cell adhesion molecule in understanding angiogenesis. Glycobiology. 2014; 24(12):1260–1264.
96. Paddock C, Zhou D, Lertkiatmongkol P, Newman PJ, Zhu J. Structural basis for PECAM-1 homophilic binding. Blood. 2016; 127:1052-1061.
97. Klagsbrun M, Takashima S, Mamluk R. The role of neuropilin in vascular and tumor biology. Bagnard D (ed), Neuropilin: From nervous System to Vascular Biology, Springer Science+Business Media New York 2002.
98. Hsieh SH, Ying NW, Wu MH, et al. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene. 2008; 27:3746–3753.
99. Lampropoulou A, Ruhrberg Ch. Neuropilin regulation of angiogenesis. Biochem Soc Trans. 2014; 42:1623–1628.
100. Aurore Dumond A, Pagès G. Neuropilins, as relevant oncology target: their role in the tumoral microenvironment. Front Cell Dev Biol. 2020; 8:662. doi: 10.3389/fcell.2020.00662.
101. Bosseboeuf E, Chikh A, Chaker AB, et al. Neuropilin-1 interacts with VE-cadherin and TGFβR2 to stabilize adherens junctions and prevent activation of endothelium under flow. Signal. 2020; 16, eabo4863.
102. Kiwaki K, Novak CM, Hsu DK, Fu-Tong Liu F-T, Levine JA. Galectin-3 stimulates preadipocyte proliferation and is up-regulated in growing adipose tissue. Obesity. 2007; 15:32–39.
103. Rhodes DH, Pini1 M, Castellanos KJ, et al. Adipose tissue specific modulation of galectin expression in lean and obese mice: evidence for regulatory function. Obesity (Silver Spring). 2013; 21(2):310–319.
104. Menini S, Iacobini C, Blasetti Fantauzzi C, Pesce CM, Pugliese G. Role of Galectin-3 in Obesity and Impaired Glucose Homeostasis. Oxidative Medicine and Cellular Longevity. 2016. doi.org/10.1155/2016/9618092.
105. Wang C, Wang Y, Ma S_R, Zuo Z-Y, Wu Y-B, Kong W-J. Berberine inhibits adipocyte differentiation, proliferation and adiposity through down-regulating galectin-3. Scientific Reports. 2019. doi.org/10.1038/s41598-019-50103-5.
106. Blasetti Fantauzzi C, Iacobini C, Menini S, Vitale M, et al. Galectin‑3 gene deletion results in defective adipose tissue maturation and impaired insulin sensitivity and glucose homeostasis. Scientific Reports. 2020 doi.org/10.1038/s41598-020-76952-z.
107. Fryk E, Silva VRR, Jansson P-A. Galectin-1 in Obesity and Type 2 Diabetes. Metabolites. 2022; 12, 930. doi.org/10.3390/metabo12100930.
108. Elias I, Franckhauser S, Ferré T, et al. Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes. 2012; 61:1801–1813.
109. AlZaim I, de Rooij LPMH, Sheikh BN, Börgeson E, Kalucka J. The evolving functions of the vasculature in regulating adipose tissue biology in health and obesity. Nat Rev Endocrinol. 2023; 19:691-707.
110. Dhumale P, Nielsen JV. Schmidt Hansen AC, et al. CD31 defines a subpopulation of human adipose‑derived regenerative cells with potent angiogenic effects. Scientific Reports. 2023; 13:14401. doi.org/10.1038/s41598-023-41535-1.
111. Monsuur HN, Weijers EM, Niessen FB, et al. Extensive characterization and comparison of endothelial cells derived from dermis and adipose tissue: potential use in tissue engineering. PLoS ONE. 2016; 11(11): e0167056. doi:10.1371/journal.pone.0167056.
112. Bix G. Iozzo RV. Novel interactions of perlecan: Unraveling perlecan’s role in angiogenesis. Microsc Res Tech. 2008; 71:339–348.
113. Zoeller JJ, Whitelock JM, Iozzo RV. Perlecan regulates developmental angiogenesis by modulating the VEGF-VEGFR2 axis. Matrix Biol. 2009; 28:284–291.
114. Rocha SF, Schiller M, Jing D, et al. Esm1 modulates endothelial tip cell behavior and vascular permeability by enhancing VEGF bioavailability. Circ Res. 2014; 115:581-590.
115. Wu M-H, Ying N-W, Hong T-M, Chiang W-F, Lin Y-T, Chen Y-L. Galectin-1 induces vascular permeability through the neuropilin-1/vascular endothelial growth factor receptor-1 complex. Angiogenesis. 2014 doi:10.1007/s10456-014-9431-8.
116. Pang H-B, Braun GB, Ruoslahti E. Neuropilin-1 and heparan sulfate proteoglycans cooperate in cellular uptake of nanoparticles functionalized by cationic cell-penetrating peptides. Sci Adv. 2015; 1:e1500821.
117. Painter ChD, Sankaranarayanan NV, Nagarajan B, et al. Alteration of neuropilin‑1 and heparan sulfate interaction impairs murine B16 tumor growth. ACS Chem Biol. 2024; 19:1820-1835.
118. Chikh A, Raimondi C. Endothelial Neuropilin-1: a multifaced signal transducer with an emerging role in inflammation and atherosclerosis beyond angiogenesis. Biochem Soc Trans. 2024; 52:137–150.
119. Christian Fischer Ch, Sanchez-Ruderisch H, Welzel M. Galectin-1 interacts with the α5β1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem. 2005; 280 (44):37266–37277.
120. Rabinovich GA, Toscano MA, Jackson D, Vasta G. Functions of cell surface galectin-glycan lattices. Curr Opin Struct Biol. 2007 ; 17:513-520.
121. Mariño KV, Cagnoni AJ, Croci DO, Rabinovich GA. Targeting galectin-driven regulatory circuits in cancer and fibrosis. Nat Rev Drugs Discovery. 2023 https://doi.org/10.1038/s41573-023-00636-2.
122. Arciniegas E, Salgado A, Carrillo LM, Rojas H, Obregón R, Moyano C. Galectin-1, -3, and -8 and their binding partners in the intussusceptive microvascular growth in lobular capillary hemangioma. In: Gokce Anik Ilhan editor. Galectin-3 and its role in human health. Nova Medicine & Health; New York, USA: 2025. P.81-107. doi.org/10.52305/VUZR1221.
123. Díaz-Alvarez L, Ortega E. The many roles of galectin-3, a multifaceted molecule, in innate immune responses against pathogens. Mediators Inflamm. 2017. doi.org/10.1155/2017/9247574.