Regulation of inflammation and fibrosis by macrophages in lymphedema

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 9, 2015, Pages H1065-H1077

  Ghanta, Swapna ^a   Cuzzone, Daniel A ^a   Torrisi, Jeremy S ^a   Albano, Nicholas J ^a   Joseph, Walter J ^a   Savetsky, Ira L ^a   Gardenier, Jason C ^a   Chang, David ^b   Zampell, Jamie C ^a   Mehrara, Babak J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

Diphtheria toxin; Fibrosis; Inflammation; Lymphatic function; Lymphedema; Macrophages

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; VASCULOTROPIN C; VASCULAR ENDOTHELIAL GROWTH FACTOR C, MOUSE; VEGFC PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BREAST CANCER; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; FIBROSIS; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; INFLAMMATION; LYMPHEDEMA; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SWELLING; TH2 CELL; WILD TYPE; ANIMAL; BIOPSY; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CASE CONTROL STUDY; DISEASE MODEL; IMMUNOLOGY; LYMPH VESSEL; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PATHOPHYSIOLOGY; TIME; WHOLE BODY RADIATION;

ANIMALS; BIOPSY; BONE MARROW TRANSPLANTATION; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; FEMALE; FIBROSIS; HUMANS; INFLAMMATION; LYMPHATIC VESSELS; LYMPHEDEMA; MACROPHAGES; MICE, INBRED C57BL; PHENOTYPE; TH2 CELLS; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR C; WHOLE-BODY IRRADIATION;

EID: 84929688875     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00598.2014     Document Type: Article

References (38)

1. Avraham T, Daluvoy S, Zampell J, Yan A, Haviv YS, Rockson SG, Mehrara BJ. Blockade of transforming growth factor-b1 accelerates lymphatic regeneration during wound repair. Am J Pathol177: 3202–3214, 2010.
2. Avraham T, Yan A, Zampell JC, Daluvoy SV, Haimovitz-Friedman A, Cordeiro AP, Mehrara BJ. Radiation therapy causes loss of dermal lymphatic vessels and interferes with lymphatic function by TGF-b1- mediated tissue fibrosis. Am J Physiol Cell Physiol299: C589–C605, 2010.
3. Avraham T, Zampell JC, Yan A, Elhadad S, Weitman ES, Rockson SG, Bromberg J, Mehrara BJ. Th2 differentiation is necessary for soft tissue fibrosis and lymphatic dysfunction resulting from lymphedema. FASEB J27: 1114–1126, 2013.
4. Clavin NW, Avraham T, Fernandez J, Daluvoy SV, Soares MA, Chaudhry A, Mehrara BJ. TGF-b1 is a negative regulator of lymphatic regeneration during wound repair. Am J Physiol Heart Circ Physiol295: H2113–H2127, 2008.
5. Cormier JN, Askew RL, Mungovan KS, Xing Y, Ross MI, Armer JM. Lymphedema beyond breast cancer: a systematic review and meta-analysis of cancer-related secondary lymphedema. Cancer116: 5138–5149, 2010.
6. Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, Wu S, Lang R, Iredale JP. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest115: 56–65, 2005.
7. Goldman J, Le TX, Skobe M, Swartz MA. Overexpression of VEGF-C causes transient lymphatic hyperplasia but not increased lymphangiogenesis in regenerating skin. Circ Res96: 1193–1199, 2005.
8. Goldman j Rutkowski J, Shields J, Pasquier M, Cui Y, Schmökel H, Willey S, Hicklin D, Pytowski B, Swartz M. Cooperative and redundant roles of VEGFR-2 and VEGFR-3 signaling in adult lymphangiogenesis. FASEB J21: 1003–1012, 2007.
9. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, MacDonald AS, Allen JE. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science332: 1284–1288, 2011.
10. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N, Ohtsuka-Kowatari N, Kumagai K, Sakamoto K, Kobayashi M, Yamauchi T, Ueki K, Oishi Y, Nishimura S, Manabe I, Hashimoto H, Ohnishi Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Nagai R, Kadowaki T. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem281: 26602–26614, 2006.
11. Machnik A, Neuhofer W, Jantsch J, Dahlmann A, Tammela T, Machura K, Park JK, Beck FX, Muller DN, Derer W, Goss J, Ziomber A, Dietsch P, Wagner H, van Rooijen N, Kurtz A, Hilgers KF, Alitalo K, Eckardt KU, Luft FC, Kerjaschki D, Titze J. Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat Med15: 545–552, 2009.
12. McLaughlin SA, Wright MJ, Morris KT, Giron GL, Sampson MR, Brockway JP, Hurley KE, Riedel ER, Van Zee KJ. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol26: 5213–5219, 2008.
13. Mihara M, Hara H, Hayashi Y, Narushima M, Yamamoto T, Todokoro T, Iida T, Sawamoto N, Araki J, Kikuchi K, Murai N, Okitsu T, Kisu I, Koshima I. Pathological steps of cancer-related lymphedema: histological changes in the collecting lymphatic vessels after lymphadenectomy. PLoS One7: e41126, 2012.
14. Mills CD. M1 and M2 macrophages: oracles of health and disease. Crit Rev Immunol32: 463–488, 2012.
15. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol11: 723–737, 2011.
16. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med15: 914–920, 2009.
17. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, Nitadori-Hoshino A, Hoffman C, Badal K, Garcia BA, Callahan MK, Yuan J, Martins VR, Skog J, Kaplan RN, Brady MS, Wolchok JD, Chapman PB, Kang Y, Bromberg J, Lyden D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med18: 883–891, 2012.
18. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, Thompson RW, Cheever AW, Murray PJ, Wynn TA. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog5: e1000371, 2009.
19. Petrek JA, Senie RT, Peters M, Rosen PP. Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer92: 1368–1377, 2001.
20. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V, Setty M, Leslie CS, Oei Y, Pedraza A, Zhang J, Brennan CW, Sutton JC, Holland EC, Daniel D, Joyce JA. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med19: 1264–1272, 2013.
21. Rockson SG. Secondary lymphedema: is it a primary disease? Lymphat Res Biol6: 63–64, 2008.
22. Rockson SG, Rivera KK. Estimating the population burden of lymphedema. Ann NY Acad Sci1131: 147–154, 2008.
23. 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 Res72: 161–171, 2006.
24. Savetsky IL, Torrisi JS, Cuzzone DA, Ghanta S, Albano NJ, Gardenier JC, Joseph WJ, Mehrara BJ. Obesity increases inflammation and impairs lymphatic function in a mouse model of lymphedema. Am J Physiol Heart Circ Physiol307: H165–H172, 2014.
25. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc3: 1101–1108, 2008.
26. Shen B, Liu X, Fan Y, Qiu J. Macrophages regulate renal fibrosis through modulating TGFbeta superfamily signaling. Inflammation15: 15, 2014.
27. 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 Surg120: 982–991, 2007.
28. Suganami T, Nishida J, Ogawa Y. A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler Thromb Vasc Biol25: 2062–2068, 2005.
29. 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 Physiol294: H1326–H1334, 2008.
30. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods174: 83–93, 1994.
31. Wang H, Melton DW, Porter L, Sarwar ZU, McManus LM, Shireman PK. Altered macrophage phenotype transition impairs skeletal muscle regeneration. Am J Pathol184: 1167–1184, 2014.
32. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest117: 524–529, 2007.
33. Wynn TA, Barron L. Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis30: 245–257, 2010.
34. Yan A, Avraham T, Zampell J, Aschen S, Mehrara B. Mechanisms of lymphatic regeneration after tissue transfer. PLoS One6: e17201, 2011.
35. Zampell J, Elhadad S, Avraham T, Weitman E, Aschen S, Yan A, Mehrara BJ. Toll-like receptor deficiency worsens inflammation and lymphedema after lymphatic injury. Am J Physiol Cell Physiol302: C709–C719, 2012.
36. Zampell JC, Yan A, Avraham T, Daluvoy S, Weitman ES, Mehrara BJ. HIF-1α coordinates lymphangiogenesis during wound healing and in response to inflammation. FASEB J26: 1027–1039, 2012.
37. Zampell JC, Yan A, Elhadad S, Avraham T, Weitman E, Mehrara BJ. CD4(+) cells regulate fibrosis and lymphangiogenesis in response to lymphatic fluid stasis. PLoS One7: e49940, 2012.
38. Zhang B, Wang J, Gao J, Guo Y, Chen X, Wang B, Gao J, Rao Z, Chen Z. Alternatively activated RAW264.7 macrophages enhance tumor lymphangiogenesis in mouse lung adenocarcinoma. J Cell Biochem107: 134–143, 2009.