Characterization of lymphangiogenesis in a model of adult skin regeneration

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 291, Issue 3, 2006, Pages

  Rutkowski, Joseph M ^a   Boardman, Kendrick C ^b   Swartz, Melody A ^a,b  

^a EPFL   (Switzerland)

^b Northwestern University   (United States)

Author keywords

Interstitial fluid flow; Lymphatic; Matrix metalloproteinase 9; Perlecan; Vasculogenesis

Indexed keywords

GELATINASE B; MATRIX METALLOPROTEINASE; PERLECAN; PROTEOHEPARAN SULFATE; VASCULOTROPIN A; VASCULOTROPIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASEMENT MEMBRANE; CELL MIGRATION; CELL REGENERATION; CONTROLLED STUDY; FEMALE; IMMUNOCOMPETENT CELL; INTERSTITIAL FLUID; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN CELL;

ANIMALS; CELL MOVEMENT; ENDOTHELIUM, LYMPHATIC; FEMALE; GENE EXPRESSION REGULATION; HEPARAN SULFATE PROTEOGLYCANS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; REGENERATION; SKIN; SKIN PHYSIOLOGY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 33748434621     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00038.2006     Document Type: Article

References (44)

1. Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, Wilks AF, Alitalo K, and Stacker SA. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 95: 548-553, 1998.
2. Achen MG, McColl BK, and Stacker SA. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7: 121-127, 2005.
3. Balbin M, Fueyo A, Knauper V, Pendas AM, Lopez JM, Jimenez MG, Murphy G, and Lopez-Otin C. Collagenase 2 (MMP-8) expression in murine tissue-remodeling processes analysis of its potential role in postpartum involution of the uterus. J Biol Chem 273: 23959-23968, 1998.
4. Boardman KC and Swartz MA. Interstitial flow as a guide for lymphangiogenesis. Circ Res 92: 801-808, 2003.
5. Cao Y, Linden P, Farnebo J, Cao R, Eriksson A, Kumar V, Qi JH, Claesson-Welsh L, and Alitalo K. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 95: 14389-14394, 1998.
6. Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology 69: 4-10, 2005.
7. Gale NW, Thurston G, Hackett SF, Renard R, Wang Q, McClain J, Martin C, Witte C, Witte MH, Jackson D, Suri C, Campochiaro PA, Wiegand SJ, and Yancopoulos GD. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell 3: 411-423, 2002.
8. Gillard JA, Reed MW, Buttle D, Cross SS, and Brown NJ. Matrix metalloproteinase activity and immunohistochemical profile of matrix metalloproteinase-2 and -9 and tissue inhibitor of metalloproteinase-1 during human dermal wound healing. Wound Repair Regen 12: 295-304, 2004.
9. Goldman J, Le TX, Skobe M, and Swartz MA. Overexpression of VEGF-C causes transient lymphatic hyperplasia but not increased lymphangiogenesis in regenerating skin. Circ Res 96: 1193-1199, 2005.
10. Haas TL, Davis SJ, and Madri JA. Three-dimensional type I collagen lattices induce coordinate expression of matrix metalloproteinases MT1-MMP and MMP-2 in microvascular endothelial cells. J Biol Chem 273: 3604-3610, 1998.
11. Jadhav U, Chigurupati S, Lakka SS, and Mohanam S. Inhibition of matrix metalloproteinase-9 reduces in vitro invasion and angiogenesis in human microvascular endothelial cells. Int J Oncol 25: 1407-1414, 2004.
12. Jeltsch M, Kaipainen A, Joukov V, Meng X, Lakso M, Rauvala H, Swartz M, Fukumura D, Jain RK, and Alitalo K. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276: 1423-1425, 1997.
13. Jiang X and Couchman JR. Perlecan and tumor angiogenesis. J Histochem Cytochem 51: 1393-1410, 2003.
14. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, and Alitalo K. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15: 290-298, 1996.
15. Kinsella MG, Tran PK, Weiser-Evans MC, Reidy M, Majack RA, and Wight TN. Changes in perlecan expression during vascular injury: role in the inhibition of smooth muscle cell proliferation in the late lesion. Arterioscler Thromb Vasc Biol 23: 608-614, 2003.
16. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, Joukov V, and Alitalo K. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122: 3829-3837, 1996.
17. Lambert V, Wielockx B, Munaut C, Galopin C, Jost M, Itoh T, Werb Z, Baker A, Libert C, Krell HW, Foidart JM, Noel A, and Rakic JM. MMP-2 and MMP-9 synergize in promoting choroidal neovascularization. FASEB J 17: 2290-2292, 2003.
18. Lijnen HR, Lupu F, Moons L, Carmeliet P, Goulding D, and Collen D. Temporal and topographic matrix metalloproteinase expression after vascular injury in mice. Thromb Haemost 81: 799-807, 1999.
19. Madlener M, Parks WC, and Werner S. Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp Cell Res 242: 201-210, 1998.
20. Maruyama K, Ii M, Cursiefen C, Jackson DG, Keino H, Tomita M, Van Rooijen N, Takenaka H, D'Amore PA, Stein-Streilein J, Losordo DW, and Streilein JW. Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 115: 2363-2372, 2005.
21. Masson V, de la Ballina LR, Munaut C, Wielockx B, Jost M, Maillard C, Blacher S, Bajou K, Itoh T, Itohara S, Werb Z, Libert C, Foidart JM, and Noel A. Contribution of host MMP-2 and MMP-9 to promote tumor vascularization and invasion of malignant keratinocytes. FASEB J 19: 234-236, 2005.
22. Moldovan NI. Role of monocytes and macrophages in adult angiogenesis: a light at the tunnel's end. J Hematother Stem Cell Res 11: 179-194, 2002.
23. Moldovan NI, Goldschmidt-Clermont PJ, Parker-Thornburg J, Shapiro SD, and Kolattukudy PE. Contribution of monocytes/macrophages to compensatory neovascularization. The drilling of metalloelastase-positive tunnels in ischemic myocardium. Circ Res 87: 378-384, 2000.
24. Nakamura ES, Koizumi K, Kobayashi M, and Saiki I. Inhibition of lymphangiogenesis-related properties of murine lymphatic endothelial cells and lymph node metastasis of lung cancer by the matrix metalloproteinase inhibitor MMI270. Cancer Sci 95: 25-31, 2004.
25. Nwomeh BC, Liang HX, Cohen IK, and Yager DR. MMP-8 is the predominant collagenase in healing wounds and nonhealing ulcers. J Surg Res 81: 189-195, 1999.
26. Oh SJ, Jeltsch MM, Birkenhager R, McCarthy JE, Weich HA, Christ B, Alitalo K, and Wilting J. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol 188: 96-109, 1997.
27. Ohno-Matsui K, Uetama T, Yoshida T, Hayano M, Itoh T, Morita I, and Mochizuki M. Reduced retinal angiogenesis in MMP-2-deficient mice. Invest Ophthalmol Vis Sci 44: 5370-5375, 2003.
28. Oliver G and Alitalo K. The lymphatic vasculature: recent progress and paradigms. Annu Rev Cell Dev Biol 21: 457-483, 2005.
29. Pytowski B, Goldman J, Persaud K, Wu Y, Witte L, Hicklin DJ, Skobe M, Boardman KC, and Swartz MA. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst 97: 14-21, 2005.
30. Salo T, Makela M, Kylmaniemi M, Autio-Harmainen H, and Larjava H. Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab Invest 70: 176-182, 1994.
31. Schacht V, Ramirez MI, Hong YK, Hirakawa S, Feng D, Harvey N, Williams M, Dvorak AM, Dvorak HF, Oliver G, and Detmar M. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J 22: 3546-3556, 2003.
32. Schoppmann SF, Birner P, Stockl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K, and Kerjaschki D. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161: 947-956, 2002.
33. Segev A, Nili N, and Strauss BH. The role of perlecan in arterial injury and angiogenesis. Cardiovasc Res 63: 603-610, 2004.
34. Sephel GC, Kennedy R, and Kudravi S. Expression of capillary basement membrane components during sequential phases of wound angiogenesis. Matrix Biol 15: 263-279, 1996.
35. Skobe M, Hamberg LM, Hawighorst T, Schirner M, Wolf GL, Alitalo K, and Detmar M. Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 159: 893-903, 2001.
36. Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 200: 448-464, 2003.
37. Swartz MA. The physiology of the lymphatic system. Adv Drug Delivery Res 50: 3-20, 2001.
38. Swartz MA, Berk DA, and Jain RK. Transport in lymphatic capillaries. I. Macroscopic measurements using residence time distribution theory. Am J Physiol Heart Circ Physiol 270: H324-H329, 1996.
39. Swartz MA and Boardman KC Jr. The role of interstitial stress in lymphatic function and lymphangiogenesis. Ann NY Acad Sci 979: 197-210, 2002.
40. Tammela T, Saaristo A, Lohela M, Morisada T, Tornberg J, Norrmen C, Oike Y, Pajusola K, Thurston G, Suda T, Yla-Herttuala S, and Alitalo K. Angiopoietin-1 promotes lymphatic sprouting and hyperplasia. Blood 105: 4642-4648, 2005.
41. Whitelock JM, Graham LD, Melrose J, Murdoch AD, Iozzo RV, and Underwood PA. Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol 18: 163-178, 1999.
42. Wigle JT and Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 98: 769-778, 1999.
43. Yuan L, Moyon D, Pardanaud L, Breant C, Karkkainen MJ, Alitalo K, and Eichmann A. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129: 4797-4806, 2002.
44. Zijlstra A, Aimes RT, Zhu D, Regazzoni K, Kupriyanova T, Seandel M, Deryugina EI, and Quigley JP. Collagenolysis-dependent angiogenesis mediated by matrix metalloproteinase-13 (collagenase-3). J Biol Chem 279: 27633-27645, 2004.