Impact of tumour associated macrophages in pancreatic cancer

BMB Reports

Volumn 46, Issue 3, 2013, Pages 131-138

  Mielgo, Ainhoa ^a   Schmid, Michael C ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Cancer; Macrophage; Myeloid cells; Pancreatic ductal adenocarcinoma; Tumour microenvironment

Indexed keywords

HUMAN; IMMUNOLOGY; MACROPHAGE; PANCREAS TUMOR; PHYSIOLOGY; SHORT SURVEY; TUMOR MICROENVIRONMENT;

HUMANS; MACROPHAGES; PANCREATIC NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84876872788     PISSN: 19766696     EISSN: 1976670X     Source Type: Journal    
DOI: 10.5483/BMBRep.2013.46.3.036     Document Type: Short Survey

References (62)

1. Raimondi, S., Maisonneuve, P. and Lowenfels, A. B. (2009) Epidemiology of pancreatic cancer: an overview. Nat. Rev. Gastroenterol. Hepatol. 6, 699-708.
2. Brune, K. A., Lau, B., Palmisano, E., Canto, M., Goggins, M. G., Hruban, R. H. and Klein, A. P. (2010) Importance of age of onset in pancreatic cancer kindreds. J. Natl. Cancer Inst. 102, 119-126.
3. Wolpin, B. M., Chan, A. T., Hartge, P., Chanock, S. J., Kraft, P., Hunter, D. J., Giovannucci, E. L. and Fuchs, C. S. (2009) ABO blood group and the risk of pancreatic cancer. J. Natl. Cancer Inst. 101, 424-431.
4. Ojajarvi, I. A., Partanen, T. J., Ahlbom, A., Boffetta, P., Hakulinen, T., Jourenkova, N., Kauppinen, T. P., Kogevinas, M., Porta, M., Vainio, H. U., Weiderpass, E. and Wesseling, C. H. (2000) Occupational exposures and pancreatic cancer: a meta-analysis. Occup. Environ. Med. 57, 316-324.
5. Winter, J. M., Brennan, M. F., Tang, L. H., D'Angelica, M. I., Dematteo, R. P., Fong, Y., Klimstra, D. S., Jarnagin, W. R. and Allen, P. J. (2012) Survival after resection of pancreatic adenocarcinoma: results from a single institution over three decades. Ann. Surg. Oncol. 19, 169-175.
6. Burris, H. A., 3rd, Moore, M. J., Andersen, J., Green, M. R., Rothenberg, M. L., Modiano, M. R., Cripps, M. C., Portenoy, R. K., Storniolo, A. M., Tarassoff, P., Nelson, R., Dorr, F. A., Stephens, C. D. and Von Hoff, D. D. (1997) Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. 15, 2403-2413.
7. Conroy, T., Desseigne, F., Ychou, M., Bouche, O., Guimbaud, R., Becouarn, Y., Adenis, A., Raoul, J. L., Gourgou-Bourgade, S., de la Fouchardiere, C., Bennouna, J., Bachet, J. B., Khemissa-Akouz, F., Pere-Verge, D., Delbaldo, C., Assenat, E., Chauffert, B., Michel, P., Montoto-Grillot, C. and Ducreux, M. (2011) FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N. Engl. J. Med. 364, 1817-1825.
8. Neoptolemos, J. P. (2011) Adjuvant treatment of pancreatic cancer. Eur. J. Cancer 47(Suppl 3), S378-380.
9. Erkan, M., Hausmann, S., Michalski, C. W., Fingerle, A. A., Dobritz, M., Kleeff, J. and Friess, H. (2012) The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat. Rev. Gastroenterol. Hepatol. 9, 454-467.
10. Olive, K. P., Jacobetz, M. A., Davidson, C. J., Gopinathan, A., McIntyre, D., Honess, D., Madhu, B., Goldgraben, M. A., Caldwell, M. E., Allard, D., Frese, K. K., Denicola, G., Feig, C., Combs, C., Winter, S. P., Ireland-Zecchini, H., Reichelt, S., Howat, W. J., Chang, A., Dhara, M., Wang, L., Ruckert, F., Grutzmann, R., Pilarsky, C., Izeradjene, K., Hingorani, S. R., Huang, P., Davies, S. E., Plunkett, W., Egorin, M., Hruban, R. H., Whitebread, N., McGovern, K., Adams, J., Iacobuzio-Donahue, C., Griffiths, J. and Tuveson, D. A. (2009) Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324, 1457-1461.
11. Erez, N., Truitt, M., Olson, P., Arron, S. T. and Hanahan, D. (2010) Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-Dependent manner. Cancer Cell 17, 135-147.
12. Beatty, G. L., Chiorean, E. G., Fishman, M. P., Saboury, B., Teitelbaum, U. R., Sun, W., Huhn, R. D., Song, W., Li, D., Sharp, L. L., Torigian, D. A., O'Dwyer, P. J. and Vonderheide, R. H. (2011) CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 331, 1612-1616.
13. Biswas, S. K. and Mantovani, A. (2010) Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11, 889-896.
14. Karp, C. L. and Murray, P. J. (2012) Non-canonical alternatives: what a macrophage is 4. J. Exp. Med. 209, 427-431.
15. Gordon, S. and Martinez, F. O. (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32, 593-604.
16. Mantovani, A. and Sica, A. (2010) Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr. Opin. Immunol. 22, 231-237.
17. Greten, F. R., Eckmann, L., Greten, T. F., Park, J. M., Li, Z. W., Egan, L. J., Kagnoff, M. F. and Karin, M. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118, 285-296.
18. Karin, M. and Greten, F. R. (2005) NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5, 749-759.
19. Lin, E. Y., Li, J. F., Gnatovskiy, L., Deng, Y., Zhu, L., Grzesik, D. A., Qian, H., Xue, X. N. and Pollard, J. W. (2006) Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66, 11238-11246.
20. Qian, B., Deng, Y., Im, J. H., Muschel, R. J., Zou, Y., Li, J., Lang, R. A. and Pollard, J. W. (2009) A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 4, e6562.
21. Ruffell, B., Affara, N. I. and Coussens, L. M. (2012) Differential macrophage programming in the tumor microenvironment. Trends Immunol. 33, 119-126.
22. Yoshikawa, K., Mitsunaga, S., Kinoshita, T., Konishi, M., Takahashi, S., Gotohda, N., Kato, Y., Aizawa, M. and Ochiai, A. (2012) Impact of tumor-associated macrophages on invasive ductal carcinoma of the pancreas head. Cancer Sci. 103, 2012-2020.
23. Sah, R. P. and Chari, S. T. (2012) Autoimmune pancreatitis: an update on classification, diagnosis, natural history and management. Curr. Gastroenterol. Rep. 14, 95-105.
24. Sah, R. P., Garg, P. and Saluja, A. K. (2012) Pathogenic mechanisms of acute pancreatitis. Curr. Opin. Gastroenterol. 28, 507-515.
25. Dugernier, T. L., Laterre, P. F., Wittebole, X., Roeseler, J., Latinne, D., Reynaert, M. S. and Pugin, J. (2003) Compartmentalization of the inflammatory response during acute pancreatitis: correlation with local and systemic complications. Am. J. Respir. Crit. Care Med. 168, 148-157.
26. Perides, G., Weiss, E. R., Michael, E. S., Laukkarinen, J. M., Duffield, J. S. and Steer, M. L. (2011) TNF-alpha-dependent regulation of acute pancreatitis severity by Ly-6C(hi) monocytes in mice. J. Biol. Chem. 286, 13327-13335.
27. Sendler, M., Dummer, A., Weiss, F. U., Kruger, B., Wartmann, T., Scharffetter-Kochanek, K., van Rooijen, N., Malla, S. R., Aghdassi, A., Halangk, W., Lerch, M. M. and Mayerle, J. (2013) Tumour necrosis factor alpha secretion induces protease activation and acinar cell necrosis in acute experimental pancreatitis in mice. Gut. 62, 430-439.
28. Infante, J. R., Matsubayashi, H., Sato, N., Tonascia, J., Klein, A. P., Riall, T. A., Yeo, C., Iacobuzio-Donahue, C. and Goggins, M. (2007) Peritumoral fibroblast SPARC expression and patient outcome with resectable pancreatic adenocarcinoma. J. Clin. Oncol. 25, 319-325.
29. Arnold, S. A., Rivera, L. B., Miller, A. F., Carbon, J. G., Dineen, S. P., Xie, Y., Castrillon, D. H., Sage, E. H., Puolakkainen, P., Bradshaw, A. D. and Brekken, R. A. (2010) Lack of host SPARC enhances vascular function and tumor spread in an orthotopic murine model of pancreatic carcinoma. Dis. Model Mech. 3, 57-72.
30. Desai, N., Trieu, V., Yao, Z., Louie, L., Ci, S., Yang, A., Tao, C., De, T., Beals, B., Dykes, D., Noker, P., Yao, R., Labao, E., Hawkins, M. and Soon-Shiong, P. (2006) Increased antitumor activity, intratumor paclitaxel concentrations, and endothelial cell transport of cremophor-free, albumin-bound paclitaxel, ABI-007, compared with cremophor-based paclitaxel. Clin. Cancer Res. 12, 1317-1324.
31. Von Hoff, D. D., Ramanathan, R. K., Borad, M. J., Laheru, D. A., Smith, L. S., Wood, T. E., Korn, R. L., Desai, N., Trieu, V., Iglesias, J. L., Zhang, H., Soon-Shiong, P., Shi, T., Rajeshkumar, N. V., Maitra, A. and Hidalgo, M. (2011) Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J. Clin. Oncol. 29, 4548-4554.
32. Rolny, C., Mazzone, M., Tugues, S., Laoui, D., Johansson, I., Coulon, C., Squadrito, M. L., Segura, I., Li, X., Knevels, E., Costa, S., Vinckier, S., Dresselaer, T., Akerud, P., De Mol, M., Salomaki, H., Phillipson, M., Wyns, S., Larsson, E., Buysschaert, I., Botling, J., Himmelreich, U., Van Ginderachter, J. A., De Palma, M., Dewerchin, M., Claesson-Welsh, L. and Carmeliet, P. (2011) HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19, 31-44.
33. Gabrilovich, D. I., Ostrand-Rosenberg, S. and Bronte, V. (2012) Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253-268.
34. Kuang, D. M., Zhao, Q., Peng, C., Xu, J., Zhang, J. P., Wu, C. and Zheng, L. (2009) Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J. Exp. Med. 206, 1327-1337.
35. Kryczek, I., Zou, L., Rodriguez, P., Zhu, G., Wei, S., Mottram, P., Brumlik, M., Cheng, P., Curiel, T., Myers, L., Lackner, A., Alvarez, X., Ochoa, A., Chen, L. and Zou, W. (2006) B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J. Exp. Med. 203, 871-881.
36. Squadrito, M. L., Pucci, F., Magri, L., Moi, D., Gilfillan, G., Ranghetti, A., Casazza, A., Mazzone, M., Lyle, R., Naldini, L. and De Palma, M. (2012) miR-511-3p Modulates Gentic Programs of Tumor-Associated Macrophages. Cell Rep. 1, 141-154.
37. Mitchem, J. B., Brennan, D. J., Knolhoff, B. L., Belt, B. A., Zhu, Y., Sanford, D. E., Belaygorod, L., Carpenter, D., Collins, L., Piwnica-Worms, D., Hewitt, S. M., Mallya Udupi, G., Gallagher, W. M., Wegner, C., West, B. L., Wang-Gillam, A., Goedegebuure, P., Linehan, D. C. and Denardo, D. G. (2013) Targeting tumor-infiltrating macrophages decreases tumor-Initiating cells, relieves immunosuppression and improves chemotherapeutic response. Cancer Res. 73, 1128-1141.
38. Bayne, L. J., Beatty, G. L., Jhala, N., Clark, C. E., Rhim, A. D., Stanger, B. Z. and Vonderheide, R. H. (2012) Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell 21, 822-835.
39. Narita, Y., Wakita, D., Ohkur, T., Chamoto, K. and Nishimura, T. (2009) Potential differentiation of tumor bearing mouse CD11b+Gr-1+ immature myeloid cells into both suppressor macrophages and immunostimulatory dendritic cells. Biomed. Res 30, 7-15.
40. Kusmartsev, S., Nagaraj, S. and Gabrilovich, D. I. (2005) Tumor-associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J. Immunol. 175, 4583-4592.
41. Lewis, J. S., Landers, R. J., Underwood, J. C., Harris, A. L. and Lewis, C. E. (2000) Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J. Pathol. 192, 150-158.
42. Sunderkotter, C., Steinbrink, K., Goebeler, M., Bhardwaj, R. and Sorg, C. (1994) Macrophages and angiogenesis. J. Leukoc. Biol. 55, 410-422.
43. Giraudo, E., Inoue, M. and Hanahan, D. (2004) An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J. Clin. Invest. 114, 623-633.
44. Hildenbrand, R., Dilger, I., Horlin, A. and Stutte, H. J. (1995) Urokinase and macrophages in tumour angiogenesis. Br. J. Cancer 72, 818-823.
45. Olson, P., Chu, G. C., Perry, S. R., Nolan-Stevaux, O. and Hanahan, D. (2011) Imaging guided trials of the angiogenesis inhibitor sunitinib in mouse models predict efficacy in pancreatic neuroendocrine but not ductal carcinoma. Proc. Natl. Acad. Sci. U.S.A. 108, E1275-1284.
46. Vincent, A., Herman, J., Schulick, R., Hruban, R. H. and Goggins, M. (2011) Pancreatic cancer. Lancet 378, 607-620.
47. Schmid, M. C., Avraamides, C. J., Dippold, H. C., Franco, I., Foubert, P., Ellies, L. G., Acevedo, L. M., Manglicmot, J. R., Song, X., Wrasidlo, W., Blair, S. L., Ginsberg, M. H., Cheresh, D. A., Hirsch, E., Field, S. J. and Varner, J. A. (2011) Receptor tyrosine kinases and TLR/IL1Rs unexpectedly activate myeloid cell PI3kgamma, a single convergent point promoting tumor inflammation and progression. Cancer Cell 19, 715-727.
48. Schmid, M. C., Avraamides, C. J., Foubert, P., Shaked, Y., Kang, S. W., Kerbel, R. S. and Varner, J. A. (2011) Combined blockade of integrin-alpha4beta1 plus cytokines SDF-1alpha or IL-1beta potently inhibits tumor inflammation and growth. Cancer Res 71, 6965-6975.
49. Tugues, S., Honjo, S., Konig, C., Noguer, O., Hedlund, M., Botling, J., Deschoemaeker, S., Wenes, M., Rolny, C., Jahnen-Dechent, W., Mazzone, M. and Claesson-Welsh, L. (2012) Genetic deficiency in plasma protein HRG enhances tumor growth and metastasis by exacerbating immune escape and vessel abnormalization. Cancer Res. 72, 1953-1963.
50. Mazzieri, R., Pucci, F., Moi, D., Zonari, E., Ranghetti, A., Berti, A., Politi, L. S., Gentner, B., Brown, J. L., Naldini, L. and De Palma, M. (2011) Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 19, 512-526.
51. Joyce, J. A. and Pollard, J. W. (2009) Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
52. Kleeff, J., Kusama, T., Rossi, D. L., Ishiwata, T., Maruyama, H., Friess, H., Buchler, M. W., Zlotnik, A. and Korc, M. (1999) Detection and localization of Mip-3alpha/LARC/ Exodus, a macrophage proinflammatory chemokine, and its CCR6 receptor in human pancreatic cancer. Int. J. Cancer 81, 650-657.
53. Campbell, A. S., Albo, D., Kimsey, T. F., White, S. L. and Wang, T. N. (2005) Macrophage inflammatory protein-3alpha promotes pancreatic cancer cell invasion. J. Surg. Res. 123, 96-101.
54. Kimsey, T. F., Campbell, A. S., Albo, D., Wilson, M. and Wang, T. N. (2004) Co-localization of macrophage inflammatory protein-3alpha (Mip-3alpha) and its receptor, CCR6, promotes pancreatic cancer cell invasion. Cancer J. 10, 374-380.
55. Stokes, J. B., Adair, S. J., Slack-Davis, J. K., Walters, D. M., Tilghman, R. W., Hershey, E. D., Lowrey, B., Thomas, K. S., Bouton, A. H., Hwang, R. F., Stelow, E. B., Parsons, J. T. and Bauer, T. W. (2011) Inhibition of focal adhesion kinase by PF-562,271 inhibits the growth and metastasis of pancreatic cancer concomitant with altering the tumor microenvironment. Mol. Cancer Ther. 10, 2135-2145.
56. Cavel, O., Shomron, O., Shabtay, A., Vital, J., Trejo-Leider, L., Weizman, N., Krelin, Y., Fong, Y., Wong, R. J., Amit, M. and Gil, Z. (2012) Endoneurial macrophages induce perineural invasion of pancreatic cancer cells by secretion of GDNF and activation of RET tyrosine kinase receptor. Cancer Res. 72, 5733-5743.
57. Schoppmann, S. F., Fenzl, A., Nagy, K., Unger, S., Bayer, G., Geleff, S., Gnant, M., Horvat, R., Jakesz, R. and Birner, P. (2006) VEGF-C expressing tumor-associated macrophages in lymph node positive breast cancer: impact on lymphangiogenesis and survival. Surgery 139, 839-846.
58. Zumsteg, A., Baeriswyl, V., Imaizumi, N., Schwendener, R., Ruegg, C. and Christofori, G. (2009) Myeloid cells contribute to tumor lymphangiogenesis. PLoS One 4, e7067.
59. Kurahara, H., Shinchi, H., Mataki, Y., Maemura, K., Noma, H., Kubo, F., Sakoda, M., Ueno, S., Natsugoe, S. and Takao, S. (2011) Significance of M2-polarized tumor-associated macrophage in pancreatic cancer. J. Surg. Res. 167, e211-219.
60. Kurahara, H., Takao, S., Maemura, K., Mataki, Y., Kuwahata, T., Maeda, K., Sakoda, M., Iino, S., Ishigami, S., Ueno, S., Shinchi, H. and Natsugoe, S. (2013) M2-Polarized tumor-associated macrophage infiltration of regional lymph nodes is associated with nodal lymphangiogenesis and occult nodal involvement in pN0 pancreatic cancer. Pancreas 42, 155-159.
61. Jinushi, M., Chiba, S., Yoshiyama, H., Masutomi, K., Kinoshita, I., Dosaka-Akita, H., Yagita, H., Takaoka, A. and Tahara, H. (2011) Tumor-associated macrophages regulate tumorigenicity and anticancer drug responses of cancer stem/initiating cells. Proc. Natl. Acad. Sci. U.S.A. 108, 12425-12430.
62. Ruffell, B., Au, A., Rugo, H. S., Esserman, L. J., Hwang, E. S. and Coussens, L. M. (2012) Leukocyte composition of human breast cancer. Proc. Natl. Acad. Sci. U.S.A. 109, 2796-2801.