Adipose-derived stem cells promote proliferation, migration, and tube formation of lymphatic endothelial cells in vitro by secreting lymphangiogenic factors

Annals of Plastic Surgery

Volumn 74, Issue 6, 2015, Pages 728-736

  Takeda, Kohsuke ^a   Sowa, Yoshihiro ^a   Nishino, Kenichi ^a   Itoh, Kyoko ^b   Fushiki, Shinji ^b  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

adipose derived stem cells; lymphangiogenesis; lymphedema

Indexed keywords

BIOLOGICAL MARKER; CULTURE MEDIUM;

ANIMAL; C57BL MOUSE; CELL MOTION; CELL PROLIFERATION; CULTURE MEDIUM; CYTOLOGY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; LYMPHANGIOGENESIS; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MOUSE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT; UPREGULATION;

ANIMALS; BIOMARKERS; CELL MOVEMENT; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; LYMPHANGIOGENESIS; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUBCUTANEOUS FAT; UP-REGULATION;

EID: 84929946367     PISSN: 01487043     EISSN: 15363708     Source Type: Journal    
DOI: 10.1097/SAP.0000000000000084     Document Type: Article

References (57)

1. Warren AG, Brorson H, Borud LJ, et al. Lymphedema: a comprehensive review. Ann Plast Surg. 2007;59:464-472.
2. Foldi E, Foldi M,Weissleder H. Conservative treatment of lymphoedema of the limbs. Angiology. 1985;36:171-180.
3. Koshima I, Inagawa K, Urushibara K, et al. Supermicrosurgical lymphaticovenular anastomosis for the treatment of lymphedema in the upper extremities. J Reconstr Microsurg. 2000;16:437-442.
4. Koshima I, Nanba Y, Tsutsui T, et al. Minimal invasive lymphaticovenular anastomosis under local anesthesia for leg lymphedema. Ann Plast Surg. 2004; 53:261-266.
5. Cooke JP. Lymphangiogenesis: a potential new therapy for lymphedema? Circulation. 2012;125:853-855.
6. Jeltsch M, Kaipainen A, Joukov V, et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 1997;276:1423-1425.
7. Makinen T, Veikkola T, Mustjoki S, et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 2001;20:4762-4773.
8. Karkkainen MJ, Saaristo A, Jussila L, et al. A model for gene therapy of human hereditary lymphedema. Proc Natl Acad Sci U S A. 2001;98:12677-12682.
9. Szuba A, Skobe M, Karkkainen MJ, et al. Therapeutic lymphangiogenesis with human recombinant VEGF-C. FASEB J. 2002;16:1985-1987.
10. Houtgraaf JH, den Dekker WK, van Dalen BM, et al. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol. 2012;59:539-540.
11. Koh KS, Oh TS, Kim H, et al. Clinical application of human adipose tissueYderived mesenchymal stem cells in progressive hemifacial atrophy (Parry- Romberg disease) with microfat grafting techniques using 3-dimensional computed tomography and 3-dimensional camera. Ann Plast Surg. 2012;69:331-337.
12. Lee MJ, Kim J, Kim MY, et al. Proteomic analysis of tumor necrosis factoralpha- induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res. 2010;9:1754-1762.
13. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211-228.
14. Sowa Y, Imura T, Numajiri T, et al. Adipose-derived stem cells produce factors enhancing peripheral nerve regeneration: influence of age and anatomic site of origin. Stem Cells Dev. 2012;21:1852-1862.
15. Yahata Y, Shirakata Y, Tokumaru S, et al. Nuclear translocation of phosphorylated STAT3 is essential for vascular endothelial growth factor-induced human dermal microvascular endothelial cell migration and tube formation. J Biol Chem. 2003;278:40026-40031.
16. Spinella F, Garrafa E, Di Castro V, et al. Endothelin-1 stimulates lymphatic endothelial cells and lymphatic vessels to grow and invade. Cancer Res. 2009; 69:2669-2676.
17. Conrad C, Niess H, Huss R, et al. Multipotent mesenchymal stem cells acquire a lymphendothelial phenotype and enhance lymphatic regeneration in vivo. Circulation. 2009;119:281-289.
18. Zhou H, Wang M, Hou C, et al. Exogenous VEGF-C augments the efficacy of therapeutic lymphangiogenesis induced by allogenic bone marrow stromal cells in a rabbit model of limb secondary lymphedema. Jpn J Clin Oncol. 2011;41:841-846.
19. Hou C,Wu X, Jin X. Autologous bone marrow stromal cells transplantation for the treatment of secondary arm lymphedema: a prospective controlled study in patients with breast cancer related lymphedema. Jpn J Clin Oncol. 2008; 38:670-674.
20. Maldonado GE, Perez CA, Covarrubias EE, et al. Autologous stem cells for the treatment of post-mastectomy lymphedema: a pilot study. Cytotherapy. 2011; 13:1249-1255.
21. Hwang JH, Kim IG, Lee JY, et al. Therapeutic lymphangiogenesis using stem cell and VEGF-C hydrogel. Biomaterials. 2011;32:4415-4423.
22. Yan A, Avraham T, Zampell JC, et al. Adipose-derived stem cells promote lymphangiogenesis in response to VEGF-C stimulation or TGF-beta1 inhibition. Future Oncol. 2011;7:1457-1473.
23. Hong YK, Lange-Asschenfeldt B, Velasco P, et al. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2beta1 integrins. FASEB J. 2004;18:1111-1113.
24. Kajiya K, Hirakawa S, Ma B, et al. Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J. 2005;24:2885-2895.
25. Shin JW, Min M, Larrieu-Lahargue F, et al. Prox1 promotes lineage-specific expression of fibroblast growth factor (FGF) receptor-3 in lymphatic endothelium: a role for FGF signaling in lymphangiogenesis. Mol Biol Cell. 2006; 17:576-584.
26. Bjorndahl M, Cao R, Nissen LJ, et al. Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc Natl Acad Sci U S A. 2005;102:15593-15598.
27. Morisada T, Oike Y, Yamada Y, et al. Angiopoietin-1 promotes LYVE-1- positive lymphatic vessel formation. Blood. 2005;105:4649-4656.
28. Gale NW, Thurston G, Hackett SF, et al. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell. 2002;3:411-423.
29. Cao R, Bjorndahl MA, Religa P, et al. PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell. 2004; 6:333-345.
30. Ning H, Liu G, Lin G, et al. Identification of an aberrant cell line among human adipose tissue-derived stem cell isolates. Differentiation. 2009;77:172-180.
31. Hsiao ST, Asgari A, Lokmic Z, et al. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem Cells Dev. 2012;21:2189-2203.
32. Lee EY, Xia Y, Kim WS, et al. Hypoxia-enhanced wound-healing function of adipose-derived stem cells: increase in stem cell proliferation and up-regulation of VEGF and bFGF. Wound Repair Regen. 2009;17:540-547.
33. Bhang SH, Cho SW, La WG, et al. Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells. Biomaterials. 2011;32:2734-2747.
34. Sadat S, Gehmert S, Song YH, et al. The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem Biophys Res Commun. 2007;363:674-679.
35. Blasi A, Martino C, Balducci L, et al. Dermal fibroblasts display similar phenotypic and differentiation capacity to fat-derived mesenchymal stem cells, but differ in anti-inflammatory and angiogenic potential. Vasc Cell. 2011;3:5.
36. Yoshimura K, Eto H, Kato H, et al. In vivo manipulation of stem cells for adipose tissue repair/reconstruction. Regen Med. 2011;6:33-41.
37. Tammela T, Saaristo A, Lohela M, et al. Angiopoietin-1 promotes lymphatic sprouting and hyperplasia. Blood. 2005;105:4642-4648.
38. Murakami M, Zheng Y, Hirashima M, et al. VEGFR1 tyrosine kinase signaling promotes lymphangiogenesis as well as angiogenesis indirectly via macrophage recruitment. Arterioscler Thromb Vasc Biol. 2008;28:658-664.
39. Kubo H, Cao R, Brakenhielm E, et al. Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc Natl Acad Sci U S A. 2002;99: 8868-8873.
40. Paupert J, Sounni NE, Noel A. Lymphangiogenesis in post-natal tissue remodeling: lymphatic endothelial cell connection with its environment. Mol Aspects Med. 2011;32:146-158.
41. Moon KM, Park YH, Lee JS, et al. The effect of secretory factors of adiposederived stem cells on human keratinocytes. Int J Mol Sci. 2012;13: 1239-1257.
42. Kumai Y, Kobler JB, Park H, et al. Crosstalk between adipose-derived stem/ stromal cells and vocal fold fibroblasts in vitro. Laryngoscope. 2009;119:799-805.
43. Zhang X, Groopman JE, Wang JF. Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin alpha5beta1. J Cell Physiol. 2005;202:205-214.
44. Zhang H, Ning H, Banie L, et al. Adipose tissue-derived stem cells secrete CXCL5 cytokine with chemoattractant and angiogenic properties. Biochem Biophys Res Commun. 2010;402:560-564.
45. Zhang H, Yang R, Wang Z, et al. Adipose tissue-derived stem cells secrete CXCL5 cytokine with neurotrophic effects on cavernous nerve regeneration. J Sex Med. 2011;8:437-446.
46. Kondo K, Shintani S, Shibata R, et al. Implantation of adipose-derived regenerative cells enhances ischemia-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2009;29:61-66.
47. NakaoN, Nakayama T, Yahata T, et al. Adipose tissue-derivedmesenchymal stem cells facilitate hematopoiesis in vitro and in vivo: advantages over bone marrowYderived mesenchymal stem cells. Am J Pathol. 2010;177:547-554.
48. Cui K, Zhao W, Wang C, et al. The CXCR4-CXCL12 pathway facilitates the progression of pancreatic cancer via induction of angiogenesis and lymphangiogenesis. J Surg Res. 2011;171:143-150.
49. Xu J, Zhang C, He Y, et al. Lymphatic endothelial cell-secreted CXCL1 stimulates lymphangiogenesis and metastasis of gastric cancer. Int J Cancer. 2012;130:787-797.
50. Wigle JT, Harvey N, Detmar M, et al. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J. 2002;21: 1505-1513.
51. Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell. 1999;98:769-778.
52. Mandriota SJ, Jussila L, Jeltsch M, et al. Vascular endothelial growth factor-Cmediated lymphangiogenesis promotes tumour metastasis. EMBO J. 2001; 20:672-682.
53. Irrthum A, Karkkainen MJ, Devriendt K, et al. Congenital hereditary lymphedema caused by a mutation that inactivates VEGFR3 tyrosine kinase. Am J Hum Genet. 2000;67:295-301.
54. Schacht V, Ramirez MI, Hong YK, et al. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 2003;22:3546-3556.
55. Mishima K, Watabe T, Saito A, et al. Prox1 induces lymphatic endothelial differentiation via integrin alpha9 and other signaling cascades. Mol Biol Cell. 2007;18:1421-1429.
56. Oka M, Iwata C, Suzuki HI, et al. Inhibition of endogenous TGF-beta signaling enhances lymphangiogenesis. Blood. 2008;111:4571-4579.
57. Choi I, Lee YS, Chung HK, et al. Interleukin-8 reduces post-surgical lymphedema formation by promoting lymphatic vessel regeneration. Angiogenesis. 2013;16:29-44.