Lymphatic function is regulated by a coordinated expression of lymphangiogenic and anti-lymphangiogenic cytokines

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 2, 2012, Pages

  Zampell, Jamie C ^a   Avraham, Tomer ^a   Yoder, Nicole ^a   Fort, Nicholas ^a   Yan, Alan ^a   Weitman, Evan S ^a   Mehrara, Babak J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Interferon ; Lymphangiogenesis; Lymphedema; Transforming growth factor 1; Vascular endothelial growth factor C

Indexed keywords

CD45 ANTIGEN; ENDOSTATIN; GAMMA INTERFERON; NEUTRALIZING ANTIBODY; TRANSFORMING GROWTH FACTOR BETA1; TUBULIN; VASCULOTROPIN A; VASCULOTROPIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; INFLAMMATION; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHEDEMA; LYMPHOSCINTIGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; WILD TYPE; WOUND HEALING;

ANIMALS; CYTOKINES; FEMALE; HEPATOCYTE GROWTH FACTOR; INFLAMMATION; INTERFERON-GAMMA; LYMPH; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; LYMPHEDEMA; MICE; MICE, INBRED C57BL; MICE, NUDE; REGENERATION; T-LYMPHOCYTES; TAIL; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

MUS; MUS MUSCULUS;

EID: 84855316492     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00306.2011     Document Type: Article

References (40)

1. Alegre ML, Tso JY, Sattar HA, Smith J, Desalle F, Cole M, Bluestone JA. An anti-murine CD3 monoclonal antibody with a low affinity for Fc gamma receptors suppresses transplantation responses while minimizing acute toxicity and immunogenicity. J Immunol 155: 1544-1555, 1995.
2. Avraham T, Clavin NW, Daluvoy SV, Fernandez J, Soares MA, Cordeiro AP, Mehrara BJ. Fibrosis is a key inhibitor of lymphatic regeneration. Plast Reconstr Surg 124: 438-450, 2009.
3. Avraham T, Daluvoy S, Zampell J, Yan A, Haviv YS, Rockson SG, Mehrara BJ. Blockade of transforming growth factor-beta1 accelerates lymphatic regeneration during wound repair. Am J Pathol 177: 3202-3214, 2010.
4. Avraham T, Yan A, Zampell J, Daluvoy S, Haimovitz-Friedman A, Cordeiro A, Mehrara B. Radiation therapy causes loss of dermal lymphatic vessels and interferes with lymphatic function by TGF-β1-mediated tissue fibrosis. Am J Physiol Cell Physiol 299: C589-C605, 2010.
5. Baker A, Kim H, Semple JL, Dumont D, Shoichet M, Tobbia D, Johnston M. Experimental assessment of pro-lymphangiogenic growth factors in the treatment of post-surgical lymphedema following lymphadenectomy. Breast Cancer Res 12: R70, 2010.
6. Barbul A, Shawe T, Rotter SM, Efron JE, Wasserkrug HL, Badawy SB. Wound healing in nude mice: a study on the regulatory role of lymphocytes in fibroplasia. Surgery 105: 764-769, 1989.
7. Boone B, Blokx W, De Bacquer D, Lambert J, Ruiter D, Brochez L. The role of VEGF-C staining in predicting regional metastasis in melanoma. Virchows Arch 453: 257-265, 2008.
8. Brideau G, Makinen MJ, Elamaa H, Tu H, Nilsson G, Alitalo K, Pihlajaniemi T, Heljasvaara R. Endostatin overexpression inhibits lymphangiogenesis and lymph node metastasis in mice. Cancer Res 67: 11528-11535, 2007.
9. Cheung L, Han J, Beilhack A, Joshi S, Wilburn P, Dua A, An A, Rockson SG. An experimental model for the study of lymphedema and its response to therapeutic lymphangiogenesis. BioDrugs 20: 363-370, 2006.
10. Clavin NW, Avraham T, Fernandez J, Daluvoy SV, Soares MA, Chaudhry A, Mehrara BJ. TGF-β1 is a negative regulator of lymphatic regeneration during wound repair. Am J Physiol Heart Circ Physiol 295: H2113-H2127, 2008.
11. Clavin NW, Avraham T, Fernandez JG, Daluvoy SV, Soares M, Chaudhry A, Mehrara BJ. TGF-β1 is a negative regulator of lymphatic regeneration during wound repair. Am J Physiol Heart Circ Physiol 295: H2113-H2127, 2008.
12. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259: 1739-1742, 1993.
13. Dong X, Zhao X, Xiao T, Tian H, Yun C. Endostar, a recombined humanized endostatin, inhibits lymphangiogenesis and lymphatic metastasis of Lewis lung carcinoma xenograft in mice. Thorac Cardiovasc Surg 59: 133-136, 2011.
14. Feng Y, Wang W, Hu J, Ma J, Zhang Y, Zhang J. Expression of VEGF-C and VEGF-D as significant markers for assessment of lymphangiogenesis and lymph node metastasis in non-small cell lung cancer. Anat Rec (Hoboken) 293: 802-812, 2010.
15. Fukumoto S, Morifuji M, Katakura Y, Ohishi M, Nakamura S. Endostatin inhibits lymph node metastasis by a down-regulation of the vascular endothelial growth factor C expression in tumor cells. Clin Exp Metastasis 22: 31-38, 2005.
16. Gawronska-Kozak B, Bogacki M, Rim JS, Monroe WT, Manuel JA. Scarless skin repair in immunodeficient mice. Wound Repair Regen 14: 265-276, 2006.
17. Goldman J, Conley KA, Raehl A, Bondy DM, Pytowski B, Swartz MA, Rutkowski JM, Jaroch DB, Ongstad EL. Regulation of lymphatic capillary regeneration by interstitial flow in skin. Am J Physiol Heart Circ Physiol 292: H2176-H2183, 2007.
18. Goldman J, Le TX, Skobe M, Swartz MA. Overexpression of VEGF-C causes transient lymphatic hyperplasia but not increased lymphangiogenesis in regenerating skin. Circ Res 96: 1193-1199, 2005.
19. Gu Y, Qi X, Guo S. Lymphangiogenesis induced by VEGF-C and VEGF-D promotes metastasis and a poor outcome in breast carcinoma: a retrospective study of 61 cases. Clin Exp Metastasis 25: 717-725, 2008.
20. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109: 1010-1017, 2007.
21. Hu X, Ivashkiv LB. Cross-regulation of signaling pathways by interferongamma: implications for immune responses and autoimmune diseases. Immunity 31: 539-550, 2009.
22. Kataru RP, Kim H, Jang C, Choi DK, Koh BI, Kim M, Gollamudi S, Kim YK, Lee SH, Koh GY. T lymphocytes negatively regulate lymph node lymphatic vessel formation. Immunity 34: 96-107, 2011.
23. Kazama S, Watanabe T, Kanazawa T, Hatano K, Nagawa H. Vascular endothelial growth factor-C (VEGF-C) is a more specific risk factor for lymph node metastasis than VEGF-D in submucosal colorectal cancer. Hepatogastroenterology 54: 71-76, 2007.
24. Kondo K, Kaneko T, Baba M, Konno H. VEGF-C and VEGF-A synergistically enhance lymph node metastasis of gastric cancer. Biol Pharm Bull 30: 633-637, 2007.
25. Lahteenvuo M, Honkonen K, Tervala T, Tammela T, Suominen E, Lahteenvuo J, Kholova I, Alitalo K, Yla-Herttuala S, Saaristo A. Growth factor therapy and autologous lymph node transfer in lymphedema. Circulation 123: 613-620, 2011.
26. Oka M, Iwata C, Suzuki HI, Kiyono K, Morishita Y, Watabe T, Komuro A, Kano MR, Miyazono K. Inhibition of endogenous TGF-beta signaling enhances lymphangiogenesis. Blood 111: 4571-4579, 2008.
27. Ongstad EL, Bouta EM, Roberts JE, Uzarski JS, Gibbs SE, Sabel MS, Cimmino VM, Roberts MA, Goldman J. Lymphangiogenesis-independent resolution of experimental edema. Am J Physiol Heart Circ Physiol 299: H46-H54, 2010.
28. Ou J, Li J, Pan F, Xie G, Zhou Q, Huang H, Liang H. Endostatin suppresses colorectal tumor-induced lymphangiogenesis by inhibiting expression of fibronectin extra domain a and integrin alpha9. J Cell Biochem 112: 2106-2114, 2011.
29. Petrek JA, Heelan MC. Incidence of breast carcinoma-related lymphedema. Cancer 83: 2776-2781, 1998.
30. Petrek JA, Senie RT, Peters M, Rosen PP. Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 92: 1368-1377, 2001.
31. Rutkowski JM, Boardman KC, Swartz MA. Characterization of lymphangiogenesis in a model of adult skin regeneration. Am J Physiol Heart Circ Physiol 291: H1402-H1410, 2006.
32. Rutkowski JM, Moya M, Johannes J, Goldman J, Swartz MA. Secondary lymphedema in the mouse tail: Lymphatic hyperplasia, VEGF-C upregulation, and the protective role of MMP-9. Microvasc Res 72: 161-171, 2006.
33. Saaristo A, Veikkola T, Tammela T, Enholm B, Karkkainen MJ, Pajusola K, Bueler H, Yla-Herttuala S, Alitalo K. Lymphangiogenic gene therapy with minimal blood vascular side effects. J Exp Med 196: 719-730, 2002.
34. Saito Y, Nakagami H, Morishita R, Takami Y, Kikuchi Y, Hayashi H, Nishikawa T, Tamai K, Azuma N, Sasajima T, Kaneda Y. Transfection of human hepatocyte growth factor gene ameliorates secondary lymphedema via promotion of lymphangiogenesis. Circulation 114: 1177-1184, 2006.
35. Suami H, Pan WR, Taylor GI. Changes in the lymph structure of the upper limb after axillary dissection: radiographic and anatomical study in a human cadaver. Plast Reconstr Surg 120: 982-991, 2007.
36. Szuba A, Skobe M, Karkkainen MJ, Shin WS, Beynet DP, Rockson NB, Dakhil N, Spilman S, Goris ML, Strauss HW, Quertermous T, Alitalo K, Rockson SG. Therapeutic lymphangiogenesis with human recombinant VEGF-C. FASEB J 16: 1985-1987, 2002.
37. Uzarski J, Drelles MB, Gibbs SE, Ongstad EL, Goral JC, McKeown KK, Raehl AM, Roberts MA, Pytowski B, Smith MR, Goldman J. The resolution of lymphedema by interstitial flow in the mouse tail skin. Am J Physiol Heart Circ Physiol 294: H1326-H1334, 2008.
38. Yan A, Avraham T, Zampell J, Aschen S, Mehrara B. Mechanisms of lymphatic regeneration after tissue transfer. PLos One 6: e17201, 2011.
39. Yoon YS, Murayama T, Gravereaux E, Tkebuchava T, Silver M, Curry C, Wecker A, Kirchmair R, Hu CS, Kearney M, Ashare A, Jackson DG, Kubo H, Isner JM, Losordo DW. VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema. J Clin Invest 111: 717-725, 2003.
40. Zampell JC, Yan A, Avraham T, Andrade V, Malliaris S, Aschen SZ, Rockson SG, Mehrara BJ. Temporal and spatial patterns of endogenous danger signal expression after wound healing and in response to lymphedema. Am J Physiol Cell Physiol 300: C1107-C1121, 2011.