Macrophage responses to hypoxia: Implications for tumor progression and anti-cancer therapies

American Journal of Pathology

Volumn 167, Issue 3, 2005, Pages 627-635

  Lewis, Claire ^a   Murdoch, Craig ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENOMEDULLIN; ALPHA STATIN; ANGIOGENESIS INHIBITOR; ANGIOPOIETIN; B7 ANTIGEN; COMBRETASTATIN A4; CYCLOOXYGENASE 2; ENDOSTATIN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GELATINASE A; GELATINASE B; GENISTEIN; GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INTERLEUKIN 10; INTERLEUKIN 8; MATRILYSIN; N ACETYLCOLCHINOL PHOSPHATE; PENTOXIFYLLINE; PLATELET DERIVED GROWTH FACTOR; PROSTAGLANDIN E2; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; ROQUINIMEX; SCATTER FACTOR; THROMBOPLASTIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; CANCER INVASION; CONTROLLED STUDY; CYTOKINE RELEASE; GENE THERAPY; HUMAN; HUMAN TISSUE; HYPOXIA; MACROPHAGE; METASTASIS; MONOCYTE; MOUSE; NONHUMAN; OXYGEN TENSION; PHENOTYPE; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; RADIOTHERAPY; REVIEW; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; TUMOR GROWTH;

EID: 24044461733     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)62038-X     Document Type: Review

References (86)

1. Ross JA, Auger MJ: The biology of the macrophage. The Macrophage, ed 2. Edited by Burke B, Lewis CE. Oxford, Oxford University Press, 2002
2. Bingle L, Brown NJ, Lewis CE: The role of tumor-associated macrophages in tumor progression: implications for new anticancer therapies. J Pathol 2002, 196:254-265
3. Murdoch C, Giannoudis A, Lewis CE: Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 2004, 104:2224-2234
4. Konur A, Kreutz M, Knuchel R, Krause SW, Andressen R: Three dimensional co-culture of human monocytes and macrophages with tumor cells: analysis of macrophage differentiation and activation. Int J Cancer 1996, 66:645-652
5. Leek RD, Harris AL: Tumor associated macrophages in breast cancer. J Mamm Gland Biol Neoplasia 2002, 7:177-189
6. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A: Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002, 23:549-555
7. Leek RD, Landers RJ, Harrism AL, Lewis CE: Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Br J Cancer 1999, 79:991-995
8. Collingridge DR, Hill SA, Chaplin DJ: Proportion of infiltrating IgG-binding immune cells predict for tumor hypoxia. Br J Cancer 2001, 84:626-630
9. Stessels F, Van den Eynden G, Van der Auwera I, Salgado R, Van den Heuvel E, Harris AL, Jackson, DG, Colpaert CG, van Marck EA, Dirix LY, Vermeulen PB: Breast adenocarcinoma liver metastases, in contrast to colorectal cancer liver metastases, display a non-angiogenic growth pattern that preserves the stroma and lacks hypoxia. Br J Cancer 2004, 90:1429-1236
10. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL: Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996, 56:4625-4629
11. Fujimoto J, Sakaguchi H, Aoki I, Tamaya T: Clinical implications of expression of interleukin 8 related to angiogenesis in uterine cervical cancers. Cancer Res 2000, 60:2632-2635
12. Heidl G, Davaris P, Zwadlo G, Jagoda MS, Duchting S, Bierhoff E, Gruter T, Krieg V, Sorg C: Association of macrophages detected with monoclonal antibody 25 F 9 with progression and pathobiological classification of gastric carcinoma. J Cancer Res Clin Oncol 1987, 113:567-572
13. Hanada T, Nakagawa M, Emoto A, Nomura T, Nasu N, Nomura Y: Prognostic value of tumor-associated macrophage count in human bladder cancer. Int J Urol 2000, 7:263-269
14. Salvesen HB, Akslen LA: Significance of tumor-associated macrophages, vascular endothelial growth factor and thrombospondin-1 expression for tumor angiogenesis and prognosis in endometrial carcinomas. Int J Cancer 1999, 84:538-543
15. Lissbrant IF, Stattin P, Wikstrom P, Damber JE, Egevad L, Bergh A: Tumor associated macrophages in human prostate cancer: relation to clinicopathological variables and survival. Int J Oncol 2000, 17:445-451
16. Hamada I, Kato M, Yamasaki T, Iwabuchi K, Watanabe T, Yamada T, Itoyama S, Ito H, Okada K: Clinical effects of tumor-associated macrophages and dendritic cells on renal cell carcinoma. Anticancer Res 2000, 22:4281-4284
17. Vaupel P, Kelleher DK, Hockel M: Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 2001, 28:29-35
18. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D: Tumor hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev 2003, 29:297-307
19. Vordermark D, Brown JM: Endogenous markers of tumor hypoxia predictors of clinical radiation resistance? Strahlenther Onkol 2003, 179:801-811
20. Ohno S, Ohno Y, Suzuki N, Kamei T, Koike K, Inagawa H, Kohchi C, Soma G-I, Inoue M: Correlation of histological localization of tumor-associated macrophages with clinicopathological features in endometrial cancer. Anticancer Res 2004, 24:3335-3342
21. Burton JL, Wells JM, Corke KP, Maitland N, Hamdy FC, Lewis CE: Macrophages accumulate in avascular, hypoxic areas of prostate tumors: implications for the targeted therapeutic gene delivery to such sites. J Pathol 2000, 192:8A
22. Negus RP, Stamp GW, Hadley J, Balkwill FR: Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C-C chemokines. Am J Pathol 1997, 150:1723-1734
23. Grimshaw MJ, Balkwill FR: Inhibition of monocyte and macrophage chemotaxis by hypoxia and inflammation - a potential mechanism. Eur J Immunol 2001, 31:480-489
24. Ashida N, Arai H, Yamasaki M, Kita T: Differential signaling for MCP-1-dependent integrin activation and chemotaxis. Ann NY Acad Sci 2001, 947:387-389
25. Wain JH, Kirby JA, Ali S: Leucocyte chemotaxis: examination of mitogen-activated protein kinase and phosphoinositide 3-kinase activation by monocyte chemoattractant proteins-1, -2, -3 and -4. Clin Exp Immunol 2002, 127:436-444
26. Sica A, Saccani A, Bottazzi B, Bernasconi S, Allavena P, Gaetano B, Fei F, LaRosa G, Scotton C, Balkwill F, Mantovani A: Defective expression of the monocyte chemotactic protein-1 receptor CCR2 in macrophages associated with human ovarian carcinoma. J Immunol 2000, 164:733-738
27. Bosco MC, Reffo G, Puppo M, Varesio L: Hypoxia inhibits the expression of the CCR5 chemokine receptor in macrophages. Cell Immunol 2004, 228:1-7
28. Semenza G: Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 2002, 64:993-998
29. Burke B, Tang N, Corke KP, Tazzyman D, Ameri K, Wells M, Lewis CE: Expression of HIF-1alpha by human macrophages: implications for the use of macrophages in hypoxia-regulated cancer gene therapy. J Pathol 2002, 196:204-212
30. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL: The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 2000, 157:411-421
31. Park SK, Dadak AM, Haase VH, Fontana L, Giaccia AJ, Johnson RS: Hypoxia-induced gene expression occurs solely through the action of hypoxia-inducible factor 1alpha (HIF-1alpha): role of cytoplasmic trapping of HIF-2alpha. Mol Cell Biol 2003, 23:4959-4971
32. Leek RD, Talks KL, Pezzella F, Turley H, Campo L, Brown NS, Bicknell R, Taylor M, Gatter KC, Harris AL: Relation of hypoxia-inducible factor-2 alpha (HIF-2 alpha) expression in tumor-infiltrative macrophages to tumor angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res 2002, 62:1326-1329
33. Onita T, Ji PG, Xuan JW, Sakai H, Kanetake H, Maxwell PH, Fong GH, Gabril MY, Moussa M, Chin JL: Hypoxia-induced, perinecrotic expression of endothelial Per-ARNT-Sim domain protein-1/hypoxia-inducible factor-2alpha correlates with tumor progression, vascularization, and focal macrophage infiltration in bladder cancer. Clin Cancer Res 2002, 8:471-480
34. Koga F, Kageyama Y, Kawakami S, Fujii Y, Hyochi N, Ando N, Takizawa T, Saito K, Iwai A, Masuda H, Kihara K: Prognostic significance of endothelial Per-Arnt-sim domain protein 1/hypoxia-inducible factor-2alpha expression in a subset of tumor associated macrophages in invasive bladder cancer. J Urol 2004, 171:1080-1084
35. White JR, Harris RA, Lee SR, Craigon MH, Binley K, Price T, Beard GL, Mundy CR, Naylor S: Genetic amplification of the transcriptional response to hypoxia as a novel means of identifying regulators of angiogenesis. Genomics 2004, 83:1-8
36. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS: HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 2003, 112:645-657
37. Kong T, Eltzschig HK, Karhausen J, Colgan SP, Shelley CS: Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of beta2 integrin gene expression. Proc Natl Acad Sci USA 2004, 101:10440-10445
38. Kawaguchi T, Veech RL, Uyeda K: Regulation of energy metabolism in macrophages during hypoxia. Roles of fructose 2,6-bisphosphate and ribose 1,5-bisphosphate. J Biol Chem 2001, 276:28554-28561
39. Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE: Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol 2003, 163:1233-1243
40. Zampetaki A, Mitsialis SA, Pfeilschifter J, Kourembanas S: Hypoxia induces macrophage inflammatory protein-2 (MIP-2) gene expression in murine macrophages via NF-kappaB: the prominent role of p42/p44 and PI3 kinase pathways. FASEB J 2004, 18:1090-1092
41. Peters CL, Morris CJ, Mappm PI, Blake DR, Lewis CE, Winrow VR: The transcription factors hypoxia-inducible factor 1alpha and Ets-1 colocalize in the hypoxic synovium of inflamed joints in adjuvant-induced arthritis. Arthritis Rheum 2004, 50:291-296
42. Yan SF, Lu J, Zou YS, Soh-Won J, Cohen DM, Buttrick PM, Cooper DR, Steinberg SF, Mackman N, Pinsky DJ, Stern DM: Hypoxia-associated induction of early growth response-1 gene expression. J Biol Chem 1999, 274:15030-15040
43. Li EY, Nguyen AV, Russell RG, Pollard JW: Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 2001, 193:727-740
44. Sweet MJ, Hume DA: M-CSF as a regulator of macrophage activation and immune responses. Arch Immunol Ther Exp 2003, 51:169-177
45. Scholl SM, Pallud C, Beuvon F, Hacene K, Stanley ER, Rohrschneider L, Tang R, Pouillart P, Lidereau R: Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J Natl Cancer Inst 1994, 86:120-126
46. Aharinejad S, Paulus P, Sioud M, Hofmann M, Zins K, Schafer R, Stanley ER, Abraham D: Colony-stimulating factor-1 blockade by antisense oligonucleotides and small interfering RNAs suppresses growth of human mammary tumor xenografts in mice. Cancer Res 2004, 64:5378-5384
47. O'Sullivan C, Lewis CE, Harris AL, McGee JO: Secretion of epidermal growth factor by macrophages associated with breast carcinoma. Lancet 1993, 342:148-149
48. Khaliq A, Jarvis-Evans J, McLeod D, Boulton M: Oxygen modulates the response of the retinal pigment epithelium to basic fibroblast growth factor and epidermal growth factor by receptor regulation. Invest Ophthalmol Vis Sci 1996, 37:436-443
49. Mazzocchi G, Malendowicz LK, Ziolkowska A, Spinazzi R, Rebuffat P, Aragona F, Ferrazzi E, Parnigotto PP, Nussdorfer GG: Adrenomedullin (AM) and AM receptor type 2 expression is up-regulated in prostate carcinomas (PC), and AM stimulates in vitro growth of a PC-derived cell line by enhancing proliferation and decreasing apoptosis rates. Int J Oncol 2004, 25:1781-1787
50. Harmey JH, Dimitriadis E, Kay E, Redmond HP, Bouchier-Hayes D: Regulation of macrophage production of vascular endothelial growth factor (VEGF) by hypoxia and transforming growth factor beta-1. Ann Surg Oncol 1998, 5:271-278
51. Xiong M, Elson G, Legarda D, Leibovich SJ: Production of vascular endothelial growth factor by murine macrophages: regulation by hypoxia, lactate, and the inducible nitric oxide synthase pathway. Am J Pathol 1998, 153:587-598
52. Lewis JS, Landers RJ, Underwood JC, Harris AL, Lewis CE: Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J Pathol 2000, 192:150-158
53. Chen J, De S, Brainard J, Byzova TV: Metastatic properties of prostate cancer cells are controlled by VEGF. Cell Commun Adhes 2004, 11:1-11
54. Huh JI, Calvo A, Stafford J, Cheung M, Kumar R, Philp D, Kleinman HK, Green JE: Inhibition of VEGF receptors significantly impairs mammary cancer growth in C3(1)/Tag transgenic mice through antiangiogenic and non-antiangiogenic mechanisms. Oncogene 2005, 24:790-800
55. Schmeisser A, Marquetant R, Illmer T, Graffy C, Garlichs CD, Bockler D, Menschikowski D, Braun-Dullaeus R, Daniel WG, Strasser RH: The expression of macrophage migration inhibitory factor 1alpha (MIF 1alpha) in human atherosclerotic plaques is induced by different proatherogenic stimuli and associated with plaque instability. Atherosclerosis 2005, 178:83-94
56. Compeau CG, Ma J, DeCampos KN, Waddell TK, Brisseau GF, Slutsky AS, Rotstein OD: In situ ischemia and hypoxia enhance alveolar macrophage tissue factor expression. Am J Respir Cell Mol Biol 1994, 11:446-455
57. Sun B, Nishihira J, Yoshiki T, Kondo M, Sato Y, Sasaki F, Todo S: Macrophage migration inhibitory factor promotes tumor invasion and metastasis via the Rho-dependent pathway. Clin Cancer Res 2005, 11:1050-1058
58. Hagemann T, Robinson SC, Schulz M, Trumper L, Balkwill FR, Binder C: Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-alpha dependent up-regulation of matrix metalloproteases. Carcinogenesis 2004, 25:1543-1549
59. Grimshaw MJ, Wilson JL, Balkwill FR: Endothelin-2 is a macrophage chemoattractant: implications for macrophage distribution in tumors. Eur J Immunol 2002, 32:2393-2400
60. Wang FQ, So J, Reierstad S, Fishman DA: Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase. Int J Cancer 2005, 114:19-31
61. Versteeg HH, Spek CA, Peppelenbosch MP, Richel DJ: Tissue factor and cancer metastasis: the role of intracellular and extracellular signaling pathways. Mol Med 2004, 10:6-11
62. Suganami E, Takagi H, Ohashi H, Suzuma K, Suzuma I, Oh H, Watanabe D, Ojima T, Suganami T, Fujio Y, Nakao K, Ogawa Y, Yoshimura N: Leptin stimulates ischemia-induced retinal neovascularization: possible role of vascular endothelial growth factor expressed in retinal endothelial cells. Diabetes 2004, 53:2443-2448
63. Huminiecki L, Gorn M, Suchting S, Poulsom R, Bicknell R: Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics 2002, 79:547-552
64. Le Jan S, Amy C, Cazes A, Monnot C, Lamande N, Favier J, Philippe J, Sibony M, Gasc JM, Corvol P, Germain S: Angiopoietin-like 4 is a proangiogenic factor produced during ischemia and in conventional renal cell carcinoma. Am J Pathol 2003, 162:1521-1528
65. Ertel W, Singh G, Morrison MH, Ayala A, Chaudry IH: Chemically induced hypotension increases PGE2 release and depresses macrophage antigen presentation. Am J Physiol 1993, 264:R655-R660
66. Murata Y, Ohteki T, Koyasu S, Hamuro J: IFN-gamma and proinflammatory cytokine production by antigen-presenting cells is dictated by intracellular thiol redox status regulated by oxygen tension. Eur J Immunol 2002, 32:2866-2873
67. Wojtowicz-Praga S: Reversal of tumor-induced immunosuppression: a new approach to cancer therapy. J Immunother 1997, 20:165-177
68. Elgert KD, Alleva DG, Mullins DW: Tumor-induced immune dysfunction: the macrophage connection. J Leukoc Biol 1998, 64:275-290
69. Leeper-Woodford SK, Mills JW: Phagocytosis and ATP levels in alveolar macrophages during acute hypoxia. Am J Respir Cell Mol Biol 1992, 6:326-334
70. Lahat N, Rahat MA, Ballan M, Weiss-Cerem L, Engelmayer M, Bitterman H: Hypoxia reduces CD80 expression on monocytes but enhances their LPS-stimulated TNF-alpha secretion. J Leukoc Biol 2003, 74:197-205
71. Albina JE, Henry Jr WL, Mastrofrancesco B, Martin BA, Reichner JS: Macrophage activation by culture in an anoxic environment. J Immunol 1995, 155:4391-4396
72. Bellocq A, Suberville S, Philippe C, Bertrand F, Perez J, Fouqueray B, Cherqui G, Baud L: Low environmental pH is responsible for the induction of nitric-oxide synthase in macrophages. Evidence for involvement of nuclear factor-kappaB activation. J Biol Chem 1998, 273:5086-5092
73. Heming TA, Dave SK, Tuazon DM, Chopram AK, Peterson JW, Bidani A: Effects of extracellular pH on tumor necrosis factor-alpha production by resident alveolar macrophages. Clin Sci (Lond) 2001, 101:267-274
74. Guida E, Stewart A: Influence of hypoxia and glucose deprivation on tumor necrosis factor-alpha and granulocyte-macrophage colony-stimulating factor expression in human cultured monocytes. Cell Physiol Biochem 1998, 8:75-88
75. Knighton DR, Hunt TK, Scheuenstuhl H, Halliday BJ, Werb Z, Banda MJ: Oxygen tension regulates the expression of angiogenesis factor by macrophages. Science 1983, 221:1283-1285
76. Crowther M, Brown NJ, Bishop ET, Lewis CE: Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J Leukoc Biol 2001, 70:478-490
77. Vujaskovic Z, Anscher MS, Feng QF, Rabbani ZN, Amin K, Samulski TS, Dewhirst MW, Haroon ZA: Radiation-induced hypoxia may perpetuate late normal tissue injury. Int J Radiat Oncol Biol Phys 2001, 50:851-855
78. Schouwink H, Oppelaar H, Ruevekamp M, van der Valk M, Hart G, Rijken P, Baas P, Stewart FA: Oxygen depletion during and after mTHPC-mediated photodynamic therapy in RIF1 and H-MESO1 tumors. Radiat Res 2003, 159:190-198
79. van Wijngaarden J, de Rooij K, van Seek E, Bernsen H, Que I, van Hinsbergh VW, Lowik C: Identification of differentially expressed genes in a renal cell carcinoma tumor model after endostatin-treatment. Lab Invest 2004, 84:1472-1483
80. Cooney MM, Ortiz J, Bukowski RM, Remick SC: Novel vascular targeting/disrupting agents: combretastatin a4 phosphate and related compounds. Curr Oncol Rep 2005, 7:90-95
81. Wachsberger PR, Burd R, Marero N, Daskalakis C, Ryan A, McCue P, Dicker AP: Effect of the tumor vascular-damaging agent, ZD6126, on the radioresponse of U87 glioblastoma. Clin Cancer Res 2005, 11:835-842
82. Staton CA, Brown NJ, Rodgers GR, Corke KP, Tazzyman S, Underwood JC, Lewis CE: Alphastatin, a 24-amino acid fragment of human fibrinogen, is a potent new inhibitor of activated endothelial cells in vitro and in vivo. Blood 2004, 103:601-606
83. Joseph IB, Isaacs JT: Macrophage role in the anti-prostate cancer response to one class of antiangiogenic agents. J Natl Cancer Inst 1998, 90:1648-1653
84. Ohno S, Ohno Y, Suzuki N, Kamei T, Koike K, Inagawa H, Kohchi C, Soma G, Inoue M: Correlation of histological localization of tumor-associated macrophages with clinicopathological features in endometrial cancer. Anticancer Res 2004, 24:3335-3342
85. Burke B, Sumner S, Maitland N, Lewis CE: Macrophages in gene therapy: cellular delivery vehicles and in vivo targets. J Leukoc Biol 2002, 72:417-428
86. Griffiths L, Binley K, Iqball S, Iqball S, Kan O, Maxwell P, Ratcliffe P, Lewis C, Harris A, Kingsman S, Naylor S: The macrophage - a novel system to deliver gene therapy to pathological hypoxta. Gene Therapy 2000, 7:255-262