Human tumors instigate granulin-expressing hematopoietic cells that promote malignancy by activating stromal fibroblasts in mice

Journal of Clinical Investigation

Volumn 121, Issue 2, 2011, Pages 784-799

  Elkabets, Moshe ^a   Gifford, Ann M ^b   Scheel, Christina ^b   Nilsson, Bjorn ^a,c   Reinhardt, Ferenc ^b   Bray, Mark Anthony ^c   Carpenter, Anne E ^c   Jirström, Karin ^d   Magnusson, Kristina ^e   Ebert, Benjamin L ^a,c   Pontén, Fredrik ^e   Weinberg, Robert A ^b,f   McAllister, Sandra S ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d LUND UNIVERSITY   (Sweden)

^e UPPSALA UNIVERSITY   (Sweden)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GRANULIN; STEM CELL ANTIGEN 1; STEM CELL FACTOR; UNCLASSIFIED DRUG;

ADENOCARCINOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BREAST CANCER; CANCER PATIENT; CANCER SURVIVAL; CELL ACTIVATION; COHORT ANALYSIS; CONTROLLED STUDY; FIBROBLAST; GENE; GENE EXPRESSION; HEMATOPOIETIC CELL; HOST; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; STROMA CELL; TUMOR CELL; TUMOR GROWTH; UPREGULATION;

ANIMALS; BONE MARROW CELLS; BREAST NEOPLASMS; CELL LINE; DISEASE PROGRESSION; FEMALE; FIBROBLASTS; HEMATOPOIETIC STEM CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; STROMAL CELLS;

EID: 79551519982     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI43757     Document Type: Article

References (73)

1. Schoenberg BS. Multiple primary malignant neoplasms. The Connecticut experience, 1935-1964. Recent Results Cancer Res. 1977;58:1-173.
2. Watanabe S, et al. Multiple primary cancers in 5,456 autopsy cases in the National Cancer Center of Japan. J Natl Cancer Inst. 1984;72(5):1021-1027.
3. Schaapveld M, et al. Risk of new primary nonbreast cancers after breast cancer treatment: a Dutch population-based study. J Clin Oncol. 2008;26(8):1239-1246.
4. Schaapveld M, et al. The impact of adjuvant therapy on contralateral breast cancer risk and the prognostic significance of contralateral breast cancer: a population based study in the Netherlands. Breast Cancer Res Treat. 2008;110(1):189-197.
5. Carmichael AR, Bendall S, Lockerbie L, Prescott R, Bates T. The long-term outcome of synchronous bilateral breast cancer is worse than metachronous or unilateral tumours. Eur J Surg Oncol. 2002;28(4):388-391.
6. Ruiterkamp J, Ernst MF, van de Poll-Franse LV, Bosscha K, Tjan-Heijnen VC, Voogd AC. Surgical resection of the primary tumour is associated with improved survival in patients with distant metastatic breast cancer at diagnosis. Eur J Surg Oncol. 2009;35(11):1146-1151.
7. Ruiterkamp J, Voogd AC, Bosscha K, Tjan-Heijnen VC, Ernst MF. Impact of breast surgery on survival in patients with distant metastases at initial presentation: a systematic review of the literature. Breast Cancer Res Treat. 2010;120(1):9-16.
8. McAllister SS, Weinberg RA. Tumor-host interactions: a far-reaching relationship. J Clin Oncol. 2010;28(26):4022-4028.
9. McAllister SS, et al. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell. 2008;133(6):994-1005.
10. Shojaei F, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol. 2007;25(8):911-920.
11. Ince TA, et al. Transformation of different human breast epithelial cell types leads to distinct tumor phenotypes. Cancer Cell. 2007;12(2):160-170.
12. Elenbaas B, et al. Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 2001;15(1):50-65. (Pubitemid 32060682)
13. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer. 2001;1(1):46-54.
14. Hirschi KK, D'Amore PA. Pericytes in the microvasculature. Cardiovasc Res. 1996;32(4):687-698.
15. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G. PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol. 2005;7(9):870-879.
16. Walker RA. The complexities of breast cancer desmoplasia. Breast Cancer Res. 2001;3(3):143-145.
17. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006;6(5):392-401.
18. Carpenter AE, et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 2006;7(10):R100.
19. Lamprecht MR, Sabatini DM, Carpenter AE. CellProfiler: free, versatile software for automated biological image analysis. Biotechniques. 2007;42(1):71-75.
20. Pazolli E, et al. Senescent stromal-derived osteopontin promotes preneoplastic cell growth. Cancer Res. 2009;69(3):1230-1239.
21. Polyak K, Kalluri R. The role of the microenvironment in mammary gland development and cancer. Cold Spring Harb Perspect Biol. 2010;2(11):a003244.
22. Ishii G, et al. Bone-marrow-derived myofibroblasts contribute to the cancer-induced stromal reaction. Biochem Biophys Res Commun. 2003;309(1):232-240.
23. Radisky DC, Kenny PA, Bissell MJ. Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem. 2007;101(4):830-839.
24. Pietras K, Pahler J, Bergers G, Hanahan D. Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med. 2008;5(1):e19.
25. Randall TD, Weissman IL. Characterization of a population of cells in the bone marrow that phenotypically mimics hematopoietic stem cells: resting stem cells or mystery population? Stem Cells. 1998;16(1):38-48.
26. Ortiz M, Wine JW, Lohrey N, Ruscetti FW, Spence SE, Keller JR. Functional characterization of a novel hematopoietic stem cell and its place in the c-Kit maturation pathway in bone marrow cell development. Immunity. 1999;10(2):173-182.
27. Kumar R, Fossati V, Israel M, Snoeck HW. Lin-Sca1+kit- bone marrow cells contain early lymphoid-committed precursors that are distinct from common lymphoid progenitors. J Immunol. 2008;181(11):7507-7513.
28. Harman BC, Northrup DL, Allman D. Resolution of unique Sca-1highc-Kit- lymphoid-biased progenitors in adult bone marrow. J Immunol. 2008;181(11):7514-7524.
29. Trowbridge JJ, Guezguez B, Moon RT, Bhatia M. Wnt3a activates dormant c-Kit(-) bone marrow-derived cells with short-term multilineage hematopoietic reconstitution capacity. Stem Cells. 2010;28(8):1379-1389.
30. Bateman A, Bennett HP. The granulin gene family: from cancer to dementia. Bioessays. 2009;31(11):1245-1254.
31. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G. Transforming growth factor-beta 1 induces alphasmooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol. 1993;122(1):103-111.
32. Serini G, Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res. 1999;250(2):273-283.
33. Chang HY, et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A. 2002;99(20):12877-12882.
34. Chang HY, et al. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol. 2004;2(2):E7.
35. Sugimoto T, et al. Growth factor-mediated interaction between tumor cells and stromal fibroblasts in an experimental model of human small-cell lung cancer. Oncol Rep. 2005;14(4):823-830.
36. Anderberg C, et al. Paracrine signaling by platelet-derived growth factor-CC promotes tumor growth by recruitment of cancer-associated fibroblasts. Cancer Res. 2009;69(1):369-378.
37. Erez N, Truitt M, Olson P, Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell. 2010;17(2):135-147.
38. Zanocco-Marani T, Bateman A, Romano G, Valentinis B, He ZH, Baserga R. Biological activities and signaling pathways of the granulin/epithelin precursor. Cancer Res. 1999;59(20):5331-5340. (Pubitemid 29504002)
39. He Z, Bateman A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J Mol Med. 2003;81(10):600-612.
40. Jones MB, et al. The granulin-epithelin precursor/PC-cell-derived growth factor is a growth factor for epithelial ovarian cancer. Clin Cancer Res. 2003;9(1):44-51.
41. Cheung ST, et al. Granulin-epithelin precursor overexpression promotes growth and invasion of hepatocellular carcinoma. Clin Cancer Res. 2004;10(22):7629-7636.
42. Ho JC, et al. Granulin-epithelin precursor as a therapeutic target for hepatocellular carcinoma. Hepatology. 2008;47(5):1524-1532.
43. Uhlen M, et al. Towards a knowledge-based human protein atlas. Nat Biotechnol. 2010;28(12):1248-1250.
44. Perou CM, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747-752.
45. Schneider BP, et al. Triple-negative breast cancer: risk factors to potential targets. Clin Cancer Res. 2008;14(24):8010-8018.
46. Kennecke H, et al. Metastatic behavior of breast cancer subtypes. J Clin Oncol. 2010;28(20):3271-3277.
47. Van Scott EJ, Reinertson RP. The modulating influence of stromal environment on epithelial cells studied in human autotransplants. J Invest Dermatol. 1961;36:109-131.
48. Eyden B, Banerjee SS, Shenjere P, Fisher C. The myofibroblast and its tumours. J Clin Pathol. 2009;62(3):236-249.
49. Mueller MM, Fusenig NE. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer. 2004;4(11):839-849.
50. Korc M. Pancreatic cancer-associated stroma production. Am J Surg. 2007;194(4 suppl):S84-S86.
51. Mahadevan D, Von Hoff DD. Tumor-stroma interactions in pancreatic ductal adenocarcinoma. Mol Cancer Ther. 2007;6(4):1186-1197.
52. Micke P, Ostman A. Tumour-stroma interaction: cancer-associated fibroblasts as novel targets in anti-cancer therapy? Lung Cancer. 2004;45 suppl 2:S163-S175.
53. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 2007;67(21):10123-10128.
54. Direkze NC, et al. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res. 2004;64(23):8492-8495.
55. Sangai T, et al. Effect of differences in cancer cells and tumor growth sites on recruiting bone marrow-derived endothelial cells and myofibroblasts in cancer-induced stroma. Int J Cancer. 2005;115(6):885-892.
56. Bellini A, Mattoli S. The role of the fibrocyte, a bone marrow-derived mesenchymal progenitor, in reactive and reparative fibroses. Lab Invest. 2007;87(9):858-870.
57. Worthley DL, et al. Human gastrointestinal neoplasia-associated myofibroblasts can develop from bone marrow-derived cells following allogeneic stem cell transplantation. Stem Cells. 2009;27(6):1463-1468.
58. Andreu P, et al. FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell. 2010;17(2):121-134.
59. Li Y, et al. B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood. 2007;109(9):3839-3848.
60. Xiao S, Su DM, Manley NR. T cell development from kit-negative progenitors in the Foxn1Delta/Delta mutant thymus. J Immunol. 2008;180(2):914-921.
61. Serrero G, Ioffe OB. Expression of PC-cell-derived growth factor in benign and malignant human breast epithelium. Hum Pathol. 2003;34(11):1148-1154.
62. Jones MB, Spooner M, Kohn EC. The granulin-epithelin precursor: a putative new growth factor for ovarian cancer. Gynecol Oncol. 2003;88(1 pt 2):S136-S139.
63. Davidson B, et al. Granulin-epithelin precursor is a novel prognostic marker in epithelial ovarian carcinoma. Cancer. 2004;100(10):2139-2147.
64. Pan CX, et al. PC cell-derived growth factor expression in prostatic intraepithelial neoplasia and prostatic adenocarcinoma. Clin Cancer Res. 2004;10(4):1333-1337.
65. Ethier SP, Mahacek ML, Gullick WJ, Frank TS, Weber BL. Differential isolation of normal luminal mammary epithelial cells and breast cancer cells from primary and metastatic sites using selective media. Cancer Res. 1993;53(3):627-635.
66. Ebert BL, et al. An erythroid differentiation signature predicts response to lenalidomide in myelodysplastic syndrome. PLoS Med. 2008;5(2):e35.
67. Irizarry RA, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249-264.
68. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article3.
69. Nilsson B, Hakansson P, Johansson M, Nelander S, Fioretos T. Threshold-free high-power methods for the ontological analysis of genome-wide gene-expression studies. Genome Biol. 2007;8(5):R74.
70. Orimo A, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121(3):335-348.
71. Kononen J, et al. Tissue microarrays for highthroughput molecular profiling of tumor specimens. Nat Med. 1998;4(7):844-847.
72. Kallioniemi OP, Wagner U, Kononen J, Sauter G. Tissue microarray technology for high-throughput molecular profiling of cancer. Hum Mol Genet. 2001;10(7):657-662.
73. Nilsson P, et al. Towards a human proteome atlas: high-throughput generation of mono-specific antibodies for tissue profiling. Proteomics. 2005;5(17):4327-4337.