Th2 differentiation is necessary for soft tissue fibrosis and lymphatic dysfunction resulting from lymphedema

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1114-1126

  Avraham, Tomer ^a   Zampell, Jamie C ^a   Yan, Alan ^a   Elhadad, Sonia ^a   Weitman, Evan S ^a   Rockson, Stanley G ^b   Bromberg, Jacqueline ^a   Mehrara, Babak J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Inflammation; Lymphangiogenesis; Lymphatic endothelial cell

Indexed keywords

GROWTH FACTOR; INTERLEUKIN 13; INTERLEUKIN 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FIBROSIS; HUMAN; HUMAN TISSUE; INFLAMMATION; LYMPH VESSEL; LYMPHEDEMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TH2 CELL; TISSUE FIBROSIS;

ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; FIBROSIS; INFLAMMATION; INTERLEUKIN-13; INTERLEUKIN-4; LYMPHEDEMA; MICE; MICE, KNOCKOUT; MICE, NUDE; TH2 CELLS;

EID: 84874625856     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-222695     Document Type: Article

References (42)

1. Pyszel, A., Malyszczak, K., Pyszel, K., Andrzejak, R., and Szuba, A. (2006) Disability, psychological distress and quality of life in breast cancer survivors with arm lymphedema. Lymphology 39, 185-192 (Pubitemid 46147798)
2. Rockson, S. G., and Rivera, K. K. (2008) Estimating the population burden of lymphedema. Ann. N. Y. Acad. Sci. 1131, 147-154 (Pubitemid 351760885)
3. Olszewski, W. L., Jamal, S., Manokaran, G., Lukomska, B., and Kubicka, U. (1993) Skin changes in filarial and non-filarial lymphoedema of the lower extremities. Trop. Med. Parasitol. 44, 40-44 (Pubitemid 23125047)
4. Suami, H., Pan, W. R., and Taylor, G. I. (2007) 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 (Pubitemid 47367896)
5. Petrek, J. A., and Heelan, M. C. (1998) Incidence of breast carcinoma-related lymphedema. Cancer 83, 2776-2781 (Pubitemid 29024266)
6. Avraham, T., Daluvoy, S., Zampell, J., Yan, A., Haviv, Y. S., Rockson, S. G., and Mehrara, B. J. (2010) Blockade of transforming growth factor-β1 accelerates lymphatic regeneration during wound repair. Am. J. Pathol. 177, 3202-3214
7. Wynn, T. A. (2008) Cellular and molecular mechanisms of fibrosis. J. Pathol. 214, 199-210 (Pubitemid 351160157)
8. Hinrichs, C. S., Watroba, N. L., Rezaishiraz, H., Giese, W., Hurd, T., Fassl, K. A., and Edge, S. B. (2004) Lymphedema secondary to postmastectomy radiation: Incidence and risk factors. Ann. Surg. Oncol. 11, 573-580 (Pubitemid 40486714)
9. Beesley, V., Janda, M., Eakin, E., Obermair, A., and Battistutta, D. (2007) Lymphedema after gynecological cancer treatment: prevalence, correlates, and supportive care needs. Cancer 109, 2607-2614 (Pubitemid 46906482)
10. Clavin, N. W., Avraham, T., Fernandez, J., Daluvoy, S. V., Soares, M. A., Chaudhry, A., and Mehrara, B. J. (2008) Tgf-β1 is a negative regulator of lymphatic regeneration during wound repair. Am. J. Physiol. Heart Circ. Physiol. 295, H2113-H2127
11. Zampell, J., Elhadad, S., Avraham, T., Weitman, E., Aschen, S., Yan, A., and Mehrara, B. J. (2012) Toll-like receptor deficiency worsens inflammation and lymphedema after lymphatic injury. Am. J. Physiol. Cell Physiol. 302, C709-C719
12. Goldman, J., Le, T. X., Skobe, M., and Swartz, M. A. (2005) Overexpression of vegf-c causes transient lymphatic hyperplasia but not increased lymphangiogenesis in regenerating skin. Circ. Res. 96, 1193-1199 (Pubitemid 40827695)
13. Zampell, J. C., Yan, A., Avraham, T., Daluvoy, S., Weitman, E. S., and Mehrara, B. J. (2012) Hif-1α coordinates lymphangiogenesis during wound healing and in response to inflammation. FASEB J. 26, 1027-1039
14. Castelino, F. V., Seiders, J., Bain, G., Brooks, S. F., King, C. D., Swaney, J. S., Lorrain, D. S., Chun, J., Luster, A. D., and Tager, A. M. (2011) Amelioration of dermal fibrosis by genetic deletion or pharmacologic antagonism of lysophosphatidic acid receptor 1 in a mouse model of scleroderma. Arthritis Rheum. 63, 1405-1415
15. Romani, L., Mencacci, A., Grohmann, U., Mocci, S., Mosci, P., Puccetti, P., and Bistoni, F. (1992) Neutralizing antibody to interleukin 4 induces systemic protection and T helper type 1-associated immunity in murine candidiasis. J. Exp. Med. 176, 19-25
16. Yang, G., Volk, A., Petley, T., Emmell, E., Giles-Komar, J., Shang, X., Li, J., Das, A. M., Shealy, D., Griswold, D. E., and Li, L. (2004) Anti-il-13 monoclonal antibody inhibits airway hyperresponsiveness, inflammation and airway remodeling. Cytokine 28, 224-232 (Pubitemid 39573497)
17. Zampell, J. C., Avraham, T., Yoder, N., Fort, N., Yan, A., Weitman, E. S., and Mehrara, B. J. (2012) Lymphatic function is regulated by a coordinated expression of lymphangiogenic and anti-lymphangiogenic cytokines. Am. J. Physiol. Cell Physiol. 302, C392-C404
18. Mankan, A. K., and Greten, F. R. (2011) Inhibiting signal transducer and activator of transcription 3. Rationality and rationale design of inhibitors. Expert Opin. Investig. Drugs 20, 1263-1275
19. Tammela, T., Saaristo, A., Holopainen, T., Lyytikka, J., Kotronen, A., Pitkonen, M., Abo-Ramadan, U., Yla-Herttuala, S., Petrova, T. V., and Alitalo, K. (2007) Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat. Med. 13, 1458-1466 (Pubitemid 350224251)
20. Zampell, J. C., Yan, A., Avraham, T., Andrade, V., Malliaris, S., Aschen, S., Rockson, S. G., and Mehrara, B. J. (2011) 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
21. Avraham, T., Clavin, N. W., Daluvoy, S. V., Fernandez, J., Soares, M. A., Cordeiro, A. P., and Mehrara, B. J. (2009) Fibrosis is a key inhibitor of lymphatic regeneration. Plast. Reconstr. Surg. 124, 438-450
22. Poulsen, L. K., and Hummelshoj, L. (2007) Triggers of ige class switching and allergy development. Ann. Med. 39, 440-456 (Pubitemid 47479265)
23. Neurath, M. F., and Finotto, S. (2011) Il-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev. 22, 83-89
24. Karlsen, T. V., Karkkainen, M. J., Alitalo, K., and Wiig, H. (2006) Transcapillary fluid balance consequences of missing initial lymphatics studied in a mouse model of primary lymphoedema. J. Physiol. 574, 583-596
25. Olszewski, W. L., Jamal, S., Lukomska, B., Manokaran, G., and Grzelak, I. (1992) Immune proteins in peripheral tissue fluidlymph in patients with filarial lymphedema of the lower limbs. Lymphology 25, 166-171 (Pubitemid 23024635)
26. Avraham, T., Yan, A., Zampell, J. C., Daluvoy, S. V., Haimovitz- Friedman, A., Cordeiro, A. P., and Mehrara, B. J. (2010) 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
27. Yoshizaki, A., Iwata, Y., Komura, K., Ogawa, F., Hara, T., Muroi, E., Takenaka, M., Shimizu, K., Hasegawa, M., Fujimoto, M., Tedder, T. F., and Sato, S. (2008) Cd19 regulates skin and lung fibrosis via toll-like receptor signaling in a model of bleomycininduced scleroderma. Am. J. Pathol. 172, 1650-1663 (Pubitemid 351793356)
28. Kataru, R. P., Kim, H., Jang, C., Choi, D. K., Koh, B. I., Kim, M., Gollamudi, S., Kim, Y. K., Lee, S. H., and Koh, G. Y. (2011) T lymphocytes negatively regulate lymph node lymphatic vessel formation. Immunity 34, 96-107
29. Tabibiazar, R., Cheung, L., Han, J., Swanson, J., Beilhack, A., An, A., Dadras, S. S., Rockson, N., Joshi, S., Wagner, R., and Rockson, S. G. (2006) Inflammatory manifestations of experimental lymphatic insufficiency. PLoS Med. 3, e254
30. Galkowska, H., and Olszewski, W. L. (1986) Cellular composition of lymph in experimental lymphedema. Lymphology 19, 139-145 (Pubitemid 17017096)
31. Foldi, E., Sauerwald, A., and Hennig, B. (2000) Effect of complex decongestive physiotherapy on gene expression for the inflammatory response in peripheral lymphedema. Lymphology 33, 19-23 (Pubitemid 30198825)
32. Schrier, D. J., Phan, S. H., and McGarry, B. M. (1983) The effects of the nude (nu/nu) mutation on bleomycin-induced pulmonary fibrosis. A biochemical evaluation. Am. Rev. Respir. Dis. 127, 614-617 (Pubitemid 13087073)
33. Xu, J., Mora, A. L., LaVoy, J., Brigham, K. L., and Rojas, M. (2006) Increased bleomycin-induced lung injury in mice deficient in the transcription factor t-bet. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L658-L667 (Pubitemid 44498477)
34. Bennuru, S., Maldarelli, G., Kumaraswami, V., Klion, A. D., and Nutman, T. B. (2010) Elevated levels of plasma angiogenic factors are associated with human lymphatic filarial infections. Am. J. Trop. Med. Hyg. 83, 884-890
35. Rutkowski, J. M., Markhus, C. E., Gyenge, C. C., Alitalo, K., Wiig, H., and Swartz, M. A. (2010) Dermal collagen and lipid deposition correlate with tissue swelling and hydraulic conductivity in murine primary lymphedema. Am. J. Pathol. 176, 1122-1129
36. Rossi, A., Weber, E., Sacchi, G., Maestrini, D., Di Cintio, F., and Gerli, R. (2007) Mechanotransduction in lymphatic endothelial cells. Lymphology 40, 102-113 (Pubitemid 350060117)
37. Aboul-Enein A, Eshmawy I, and Arafa SA, A. (1984) The role of lymphovenous communication in the development of post mastectomy lymphedema. Surgery 95, 562
38. Nakamura, K., Radhakrishnan, K., Wong, Y. M., and Rockson, S. G. (2009) Anti-inflammatory pharmacotherapy with ketoprofen ameliorates experimental lymphatic vascular insufficiency in mice. PLoS One 4, e8380
39. Goldman j, Rutkowski, J., Shields, J., Pasquier, M., Cui, Y., Schmökel, H., Willey, S., Hicklin, D., Pytowski, B., and Swartz, M. (2007) Cooperative and redundant roles of VEGFR-2 and VEGFR-3 signaling in adult lymphangiogenesis. FASEB J. 21, 1003-1012 (Pubitemid 46495690)
40. Rutkowski, J. M., Moya, M., Johannes, J., Goldman, J., and Swartz, M. A. (2006) Secondary lymphedema in the mouse-tail: Lymphatic hyperplasia, VEGF-C upregulation, and the protective role of MMP-9. Microvasc. Res. 72, 161-171 (Pubitemid 44692751)
41. Oka, M., Iwata, C., Suzuki, H. I., Kiyono, K., Morishita, Y., Watabe, T., Komuro, A., Kano, M. R., and Miyazono, K. (2008) Inhibition of endogenous TGF-β signaling enhances lymphangiogenesis. Blood 111, 4571-4579
42. Gu, Y., Qi, X., Guo, S. (2008) 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