Apoptosis-induced CXCL5 accelerates inflammation and growth of prostate tumor metastases in bone

Journal of Clinical Investigation

Volumn 128, Issue 1, 2018, Pages 248-266

  Roca, Hernan ^a   Jones, Jacqueline D ^a   Purica, Marta C ^a   Weidner, Savannah ^a   Koh, Amy J ^a   Kuo, Robert ^b   Wilkinson, John E ^c   Wang, Yugang ^c   Daignault Newton, Stephanie ^b   Pienta, Kenneth J ^d   Morgan, Todd M ^c   Keller, Evan T ^b,c   Nör, Jacques E ^b,c   Shea, Lonnie D ^b   McCauley, Laurie K ^a,b,c  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; CXCL1 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; STAT3 PROTEIN; TRANSCRIPTION FACTOR RELA; CXCL5 PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BONE DESTRUCTION; BONE MARROW CELL; BONE MARROW DERIVED MACROPHAGE; BONE METASTASIS; CANCER GROWTH; CONTROLLED STUDY; DNA BINDING; EFFEROCYTOSIS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INFLAMMATORY CELL; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RM1 CELL LINE; TUMOR MICROENVIRONMENT; VERTEBRA BODY; ANIMAL; BONE TUMOR; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGY; METASTASIS; PATHOLOGY; PROSTATE TUMOR; SECONDARY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; BONE NEOPLASMS; CELL LINE, TUMOR; CHEMOKINE CXCL5; INFLAMMATION; MALE; MICE; MYELOID CELLS; NEOPLASM METASTASIS; NEOPLASM PROTEINS; NEOPLASMS, EXPERIMENTAL; PHAGOCYTOSIS; PROSTATIC NEOPLASMS;

EID: 85040199990     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI92466     Document Type: Article

References (65)

1. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer. 2011;11(6):411–425.
2. Roodman GD. Mechanisms of bone metastasis. N Engl J Med. 2004;350(16):1655–1664.
3. Mantovani A. La mala educación of tumor-associated macrophages: diverse pathways and new players. Cancer Cell. 2010;17(2):111–112.
4. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454(7203):436–444.
5. Lu X, et al. VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging α4β1-positive osteoclast progenitors. Cancer Cell. 2011;20(6):701–714.
6. Chen Q, Zhang XH, Massagué J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell. 2011;20(4):538–549.
7. Roca H, McCauley LK. Inflammation and skeletal metastasis. Bonekey Rep. 2015;4:706.
8. Germano G, Mantovani A, Allavena P. Targeting of the innate immunity/inflammation as complementary anti-tumor therapies. Ann Med. 2011;43(8):581–593.
9. Soki FN, et al. Bone marrow macrophages support prostate cancer growth in bone. Oncotarget. 2015;6(34):35782–35796.
10. Mills CD, Lenz LL, Harris RA. A breakthrough: macrophage-directed cancer immunotherapy. Cancer Res. 2016;76(3):513–516.
11. Gregory CD, Pound JD. Cell death in the neigh-bourhood: direct microenvironmental effects of apoptosis in normal and neoplastic tissues. JPathol. 2011;223(2):177–194.
12. Soki FN, et al. Polarization of prostate cancer-associated macrophages is induced by milk fat globule-EGF factor 8 (MFG-E8)-mediated efferocytosis. JBiolChem. 2014;289(35):24560–24572.
13. Stanford JC, et al. Efferocytosis produces a prometastatic landscape during postpartum mammary gland involution. J Clin Invest. 2014;124(11):4737–4752.
14. Michalski MN, Koh AJ, Weidner S, Roca H, McCauley LK. Modulation of osteoblastic cell efferocytosis by bone marrow macrophages. JCellBiochem. 2016;117(12):2697–2706.
15. McCabe NP, Madajka M, Vasanji A, Byzova TV. Intraosseous injection of RM1 murine prostate cancer cells promotes rapid osteolysis and periosteal bone deposition. Clin Exp Metastasis. 2008;25(5):581–590.
16. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol. 1979;17(1):16–23.
17. Shiozawa Y, et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. JClin Invest. 2011;121(4):1298–1312.
18. Acharyya S, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell. 2012;150(1):165–178.
19. Erez N, Truitt M, Olson P, Arron ST, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-κB-dependent manner. Cancer Cell. 2010;17(2):135–147.
20. Weiss MS, et al. Dynamic transcription factor activity and networks during ErbB2 breast onco-genesis and targeted therapy. Integr Biol (Camb). 2014;6(12):1170–1182.
21. Iwanaszko M, Kimmel M. NF-κB and IRF pathways: cross-regulation on target genes promoter level. BMCGenomics. 2015;16:307.
22. Moschonas A, Ioannou M, Eliopoulos AG. CD40 stimulates a “feed-forward” NF-κB-driven molecular pathway that regulates IFN-β expression in carcinoma cells. JImmunol. 2012;188(11):5521–5527.
23. Nör JE, Hu Y, Song W, Spencer DM, Núñez G. Ablation of microvessels in vivo upon dimerization of iCaspase-9. Gene Ther. 2002;9(7):444–451.
24. Yu H, Lee H, Herrmann A, Buettner R, Jove R. Revisiting STAT3 signalling in cancer: new and unexpected biological functions. Nat Rev Cancer. 2014;14(11):736–746.
25. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798–809.
26. Schust J, Sperl B, Hollis A, Mayer TU, Berg T. Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem Biol. 2006;13(11):1235–1242.
27. Jeong JH, Park SJ, Dickinson SI, Luo JL. A constitutive intrinsic inflammatory signaling circuit composed of miR-196b, Meis2, PPP3CC, and p65 drives prostate cancer castration resistance. MolCell. 2017;65(1):154–167.
28. Pierce JW, et al. Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. JBiol Chem. 1997;272(34):21096–21103.
29. Miller SC, et al. Identification of known drugs that act as inhibitors of NF-κB signaling and their mechanism of action. Biochem Pharmacol. 2010;79(9):1272–1280.
30. Davies LC, et al. Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat Commun. 2013;4:1886.
31. Jung Y, et al. Prevalence of prostate cancer metastases after intravenous inoculation provides clues into the molecular basis of dormancy in the bone marrow microenvironment. Neoplasia. 2012;14(5):429–439.
32. Begley LA, et al. CXCL5 promotes prostate cancer progression. Neoplasia. 2008;10(3):244–254.
33. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010;11(10):889–896.
34. + CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 2004;6(4):409–421.
35. Park SI, et al. Parathyroid hormone-related protein drives a CD11b+Gr1+ cell-mediated positive feedback loop to support prostate cancer growth. Cancer Res. 2013;73(22):6574–6583.
36. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 2003;19(1):71–82.
37. Caillou B, et al. Tumor-associated macrophages (TAMs) form an interconnected cellular supportive network in anaplastic thyroid carcinoma. PLoS One. 2011;6(7):e22567.
38. Mei J, et al. CXCL5 regulates chemokine scavenging and pulmonary host defense to bacterial infection. Immunity. 2010;33(1):106–117.
39. Wong KL, et al. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood. 2011;118(5):e16–e31.
40. Frankenberger M, et al. Transcript profiling of CD16-positive monocytes reveals a unique molecular fingerprint. Eur J Immunol. 2012;42(4):957–974.
41. Cros J, et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity. 2010;33(3):375–386.
42. van de Veerdonk FL, Netea MG. Diversity: a hallmark of monocyte society. Immunity. 2010;33(3):289–291.
43. Hol J, Wilhelmsen L, Haraldsen G. The murine IL-8 homologues KC, MIP-2, and LIX are found in endothelial cytoplasmic granules but not in Weibel-Palade bodies. J Leukoc Biol. 2010;87(3):501–508.
44. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemo-attractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol. 2006;8(12):1369–1375.
45. Sottnik JL, Dai J, Zhang H, Campbell B, Keller ET. Tumor-induced pressure in the bone microenvironment causes osteocytes to promote the growth of prostate cancer bone metastases. Cancer Res. 2015;75(11):2151–2158.
46. Rutkowski MR, et al. Microbially driven TLR5-dependent signaling governs distal malignant progression through tumor-promoting inflammation. Cancer Cell. 2015;27(1):27–40.
47. Lee H, Deng J, Xin H, Liu Y, Pardoll D, Yu H. A requirement of STAT3 DNA binding precludes Th-1 immunostimulatory gene expression by NF-κB in tumors. Cancer Res. 2011;71(11):3772–3780.
48. Yang M, Liu J, Piao C, Shao J, Du J. ICAM-1 suppresses tumor metastasis by inhibiting macrophage M2 polarization through blockade of efferocytosis. Cell Death Dis. 2015;6:e1780.
49. + peripheral blood mononuclear cells and induce M2-type macrophage polarization. JBiolChem. 2009;284(49):34342–34354.
50. Ju X, et al. Novel oncogene-induced metastatic prostate cancer cell lines define human prostate cancer progression signatures. Cancer Res. 2013;73(2):978–989.
51. Koh CM, Bieberich CJ, Dang CV, Nelson WG, Yegnasubramanian S, De Marzo AM. MYC and prostate cancer. Genes Cancer. 2010;1(6):617–628.
52. Sung SY, et al. Coevolution of prostate cancer and bone stroma in three-dimensional coculture: implications for cancer growth and metastasis. Cancer Res. 2008;68(23):9996–10003.
53. Hsu YL, Hou MF, Kuo PL, Huang YF, Tsai EM. Breast tumor-associated osteoblast-derived CXCL5 increases cancer progression by ERK/ MSK1/Elk-1/snail signaling pathway. Oncogene. 2013;32(37):4436–4447.
54. Highfill SL, et al. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. SciTranslMed. 2014;6(237):237ra67.
55. Nemeth Z, et al. Alterations of tumor microenvironment by carbon monoxide impedes lung cancer growth. Oncotarget. 2016;7(17):23919–23932.
56. Larson SR, et al. Characterization of osteoblastic and osteolytic proteins in prostate cancer bone metastases. Prostate. 2013;73(9):932–940.
57. + subset and soluble CD14 as biological markers of inflammatory systemic diseases and monitoring immunosuppressive therapy. Clin Chem Lab Med. 1999;37(3):209–213.
58. Subimerb C, et al. Circulating CD14(+) CD16(+) monocyte levels predict tissue invasive character of cholangiocarcinoma. Clin Exp Immunol. 2010;161(3):471–479.
59. Mukherjee R, Kanti Barman P, Kumar Thatoi P, Tripathy R, Kumar Das B, Ravindran B. Non-classical monocytes display inflammatory features: validation in sepsis and systemic lupus erythematous. SciRep. 2015;5:13886.
60. Zlotnik A, Yoshie O. The chemokine superfamily revisited. Immunity. 2012;36(5):705–716.
61. Liu Q, et al. Interleukin-1β promotes skeletal colonization and progression of metastatic prostate cancer cells with neuroendocrine features. Cancer Res. 2013;73(11):3297–3305.
62. Yang YH, et al. Semaphorin 4D promotes skeletal metastasis in breast cancer. PLoS One. 2016;11(2):e0150151.
63. Baley PA, Yoshida K, Qian W, Sehgal I, Thompson TC. Progression to androgen insensitivity in a novel in vitro mouse model for prostate cancer. J Steroid Biochem Mol Biol. 1995;52(5):403–413.
64. Thompson TC, Southgate J, Kitchener G, Land H. Multistage carcinogenesis induced by ras and myc oncogenes in a reconstituted organ. Cell. 1989;56(6):917–930.
65. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. StatApplGenetMol Biol. 2004;3(1):https://doi.org/10.2202/1544-6115.1027.