Parathyroid hormone-related protein drives a CD11b+Gr1 + cell-mediated positive feedback loop to support prostate cancer growth

Cancer Research

Volumn 73, Issue 22, 2013, Pages 6574-6583

  Park, Serk In ^a,b,c   Lee, Changki ^a   David Sadler, W ^c   Koh, Amy J ^c   Jones, Jacqueline ^c   Seo, Jung Won ^a   Soki, Fabiana N ^c   Cho, Sun Wook ^c   Daignault, Stephanie D ^d   McCauley, Laurie K ^c,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

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

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; GELATINASE B; INTERLEUKIN 6; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; PARATHYROID HORMONE RELATED PROTEIN; PARATHYROID HORMONE RELATED PROTEIN ANTIBODY; PROTEIN ANTIBODY; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CANCER GROWTH; CANCER MODEL; CAPILLARY DENSITY; CARCINOGENESIS; CD11B+GR1+ BONE MARROW DERIVED CELL; CELL ACTIVITY; CELL ISOLATION; CELL TRANSPORT; CONTROLLED STUDY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OSTEOBLAST; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, SURFACE; BONE MARROW CELLS; CELL LINE, TUMOR; CELL PROLIFERATION; DOGS; FEEDBACK, PHYSIOLOGICAL; HUMANS; MALE; MICE; MICE, NUDE; PARATHYROID HORMONE-RELATED PROTEIN; PROSTATIC NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84888382080     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4692     Document Type: Article

References (50)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
2. Shiao SL, Ganesan AP, Rugo HS, Coussens LM. Immune microenvironments in solid tumors: new targets for therapy. Gene Dev 2011;25:2559-72.
3. Park SI, Soki FN, McCauley LK. Roles of bone marrow cells in skeletal metastases: no longer bystanders. Cancer Microenviron 2011;4:237-46.
4. Park SI, Liao J, Berry JE, Li X, Koh AJ, Michalski ME, et al. Cyclophosphamide creates a receptive microenvironment for prostate cancer skeletal metastasis. Cancer Res 2012;72:2522 -32.
5. Yang L, Edwards CM, Mundy GR. Gr-1+CD11b+ myeloid-derived suppressor cells: formidable partners in tumor metastasis. J Bone Miner Res 2010;25:1701-6.
6. Youn J-I, Gabrilovich DI. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 2010;40:2969-75.
7. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004;6:409-21. (Pubitemid 39361441)
8. Zhao F, Obermann S, Wasielewski von R, Haile L, Manns MP, Korangy F, et al. Increase in frequency of myeloid-derived suppressor cells in mice with spontaneous pancreatic carcinoma. Immunology 2009;128:141-9.
9. Ahn G-O, Brown JM. Influence of bone marrow-derived hematopoietic cells on the tumor response to radiotherapy: experimental models and clinical perspectives. Cell Cycle 2009;8:970-6.
10. Ahn G-O, Tseng D, Liao C-H, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci U S A 2010;107:8363-8.
11. Shojaei F, Wu X, Malik AK, Zhong C, Baldwin ME, Schanz S, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol 2007;25:911-20. (Pubitemid 47236916)
12. Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M, et al. Abrogation of TGF beta signaling inmammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008;13:23-35. (Pubitemid 350309741)
13. Schmid MC, Avraamides CJ, Dippold HC, Franco I, Foubert P, Ellies LG, et al. Receptor tyrosine kinases and TLR/IL1Rs unexpectedly activate myeloid cell PI3kγ, a single convergent point promoting tumor inflammation and progression. Cancer Cell 2011;19:715-27.
14. Dayyani F, Gallick GE, Logothetis CJ, Corn PG. Novel therapies for metastatic castrate-resistant prostate cancer. J Natl Cancer Inst 2011;103:1665-75.
15. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011;11:411-25.
16. Li X, Loberg R, Liao J, Ying C, Snyder LA, Pienta KJ, et al. A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res 2009;69:1685- 92.
17. Liao J, Li X, Koh AJ, Berry JE, Thudi N, Rosol TJ, et al. Tumor expressed PTHrP facilitates prostate cancer-induced osteoblastic lesions. Int J Cancer 2008;123:2267-78.
18. Li J, Karaplis AC, Huang DC, Siegel PM, Camirand A, Yang XF, et al. PTHrP drives breast tumor initiation, progression, and metastasis in mice and is a potential therapy target. J Clin Invest 2011;121:4655-69.
19. Park SI, McCauley LK. Nuclear localization of parathyroid hormonerelated peptide confers resistance to anoikis in prostate cancer cells. Endocr Relat Cancer 2012;19:243-54.
20. Park SI, Kim SJ, McCauley LK, Gallick GE. Pre-clinical mouse models of human prostate cancer and their utility in drug discovery. Curr Protoc Pharmacol 2010;Chapter 14:Unit14.15.
21. Jung Y, Shiozawa Y, Wang J, McGregor N, Dai J, Park SI, 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;14:429-39.
22. Tomayko MMM, Reynolds CPC. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989;24:148- 54.
23. Pirih FQ, Michalski MN, Cho SW, Koh AJ, Berry JE, Ghaname E, et al. Parathyroid hormone mediates hematopoietic cell expansion through interleukin-6. PLoS One 2010;5:e13657.
24. Park SI, Zhang J, Phillips KA, Araujo JC, Najjar AM, Volgin AY, et al. Targeting SRC family kinases inhibits growth and lymph node metastases of prostate cancer in an orthotopic nude mouse model. Cancer Res 2008;68:3323-33.
25. Novince CM, Koh AJ, Michalski MN, Marchesan JT, Wang J, Jung Y, et al. Proteoglycan 4, a novel immunomodulatory factor, regulates parathyroid hormone actions on hematopoietic cells. Am J Pathol 2011;179:2431-42.
26. Dougherty KM, Blomme EA, Koh AJ, Henderson JE, Pienta KJ, Rosol TJ, et al. Parathyroid hormone-related protein as a growth regulator of prostate carcinoma. Cancer Res 1999;59:6015-22. (Pubitemid 30004967)
27. Tovar Sepulveda VA, Falzon M. Parathyroid hormone-related protein enhances PC-3 prostate cancer cell growth via both autocrine/paracrine and intracrine pathways. Regul Pept 2002;105:109-20. (Pubitemid 34219392)
28. Ahn G-O, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 2008;13:193-205. (Pubitemid 351318369)
29. LeRoy BE, Thudi NK, Nadella MVP, Toribio RE, Tannehill-Gregg SH, van Bokhoven A, et al. New bone formation and osteolysis by a metastatic, highly invasive canine prostate carcinoma xenograft. Prostate 2006;66:1213-22. (Pubitemid 44175343)
30. Abe F, Dafferner AJ, Donkor M, Westphal SN, Scholar EM, Solheim JC, et al. Myeloid-derived suppressor cells inmammary tumor progression in FVB Neu transgenic mice. Cancer Immunol Immunother 2010;59:47-62.
31. Kujawski M, Kortylewski M, Lee H, Herrmann A, Kay H, Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest 2008;118:3367-77.
32. Liang W, Kujawski M, Wu J, Lu J, Herrmann A, Loera S, et al. Antitumor activity of targeting SRC kinases in endothelial and myeloid cell compartments of the tumor microenvironment. Clin Cancer Res 2010;16:924-35.
33. Huang YF, Harrison JR, Lorenzo JA, Kream BE. Parathyroid hormone induces interleukin-6 heterogeneous nuclear and messenger RNA expression in murine calvarial organ cultures. Bone 1998;23:327-32. (Pubitemid 28454624)
34. Lowik CW, van der Pluijm G, Bloys H, Hoekman K, Bijvoet OL, Aarden LA, et al. Parathyroid hormone (PTH) and PTH-like protein (PLP) stimulate interleukin-6 production by osteogenic cells: a possible role of interleukin-6 in osteoclastogenesis. Biochem Biophys Res Commun 1989;162:1546-52. (Pubitemid 19214760)
35. Esbrit P, Alvarez-Arroyo MV, De Miguel F, Martin O, Martinez ME, Caramelo C. C-terminal parathyroid hormone-related protein increases vascular endothelial growth factor in human osteoblastic cells. J Am Soc Nephrol 2000;11:1085-92. (Pubitemid 30367938)
36. Sabbota AL, Kim H-RC, Zhe X, Fridman R, Bonfil RD, Cher ML. Shedding of RANKL by tumor-associated MT1-MMP activates Src-dependent prostate cancer cell migration. Cancer Res 2010;70:5558-66.
37. Hallek M, Neumann C, Schaffer M, Danhauser-Riedl S, Bubnoff von N, de Vos G, et al. Signal transduction of interleukin-6 involves tyrosine phosphorylation of multiple cytosolic proteins and activation of Srcfamily kinases Fyn, Hck, and Lyn in multiple myeloma cell lines. Exp Hematol 1997;25:1367-77. (Pubitemid 28015614)
38. Inngjerdingen M, Torgersen KM, Maghazachi AA. Lck is required for stromal cell-derived factor 1a (CXCL12)-induced lymphoid cell chemotaxis. Blood 2002;99:4318-25. (Pubitemid 34627196)
39. Jin R, Sterling JA, Edwards JR, DeGraff DJ, Lee C, Park SI, et al. Activation of NF-κ Bsignaling promotes growth of prostate cancer cells in bone.Wang QJ, editor. PLoS One 2013;8:e60983.
40. Youn J-I, Kumar V, Collazo M, Nefedova Y, Condamine T, Cheng P, et al. Epigenetic silencing of retinoblastoma gene regulates pathologic differentiation of myeloid cells in cancer. Nat Immunol 2013: 14:211-20.
41. Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 2010;176:1564-76.
42. Shojaei F, Zhong C, Wu X, Yu L, Ferrara N. Role of myeloid cells in tumor angiogenesis and growth. Trends Cell Biol 2008;18:372-8.
43. Li X, Koh AJ, Wang Z, Soki FN, Park SI, Pienta KJ, et al. Inhibitory effects of megakaryocytic cells in prostate cancer skeletal metastasis. J Bone Miner Res 2011;26:125- 34.
44. Li X, Liao J, Park SI, Koh AJ, Sadler WD, Pienta KJ, et al. Drugs which inhibit osteoclast function suppress tumor growth through calcium reduction in bone. Bone 2011;48:1354-61.
45. Kremer R, Li J, Camirand A, Karaplis AC. Parathyroid hormone related protein (PTHrP) in tumor progression. Adv Exp Med Biol 2011;720: 145- 60.
46. Zhang H, Yu C, Dai J, Keller JM, Hua A, Sottnik JL, et al. Parathyroid hormone-related protein inhibits DKK1 expression through c-Jun-mediated inhibition of β-catenin activationof the DKK1 promoter in prostate cancer. Oncogene 2013 Jun 10.
47. McCauley LK, Martin TJ. Twenty-five years of PTHrP progress: from cancer hormone to multifunctional cytokine. J Bone Miner Res 2012;27:1231-9.
48. Cho SW, Pirih FQ, Koh AJ, Michalski M, Eber MR, Ritchie K, et al. The soluble interleukin-6 receptor is a mediator of hematopoietic and skeletal actions of parathyroid hormone. J Biol Chem 2013;288: 6814- 25.
49. Guise TA, Yin JJ, Taylor SD, Kumagai Y, Dallas M, Boyce BF, et al. Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J Clin Invest 1996;98:1544-9. (Pubitemid 26327863)
50. Kim MP, Park SI, Kopetz S, Gallick GE. Src family kinases as mediators of endothelial permeability: effects on inflammation and metastasis. Cell Tissue Res 2009;335:249-59.