Elevated CXCL1 expression in breast cancer stroma predicts poor prognosis and is inversely associated with expression of TGF-β signaling proteins

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Zou, An ^a   Lambert, Diana ^a   Yeh, Henry ^a   Yasukawa, Ken ^b   Behbod, Fariba ^a   Fan, Fang ^a   Cheng, Nikki ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b BELOIT COLLEGE   (United States)

Author keywords

Breast Cancer; Chemokine; CXCL1; Fibroblast; Prognosis; SMAD2; SMAD3; Stroma; TGF beta

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALVASCULIN; CXCL1 CHEMOKINE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; PROTEIN BINDING; TUMOR MARKER;

ADULT; ANIMAL CELL; ARTICLE; BREAST CARCINOMA; CANCER GRADING; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CXCL1 GENE; DATA MINING; DOWN REGULATION; FEMALE; FIBROBLAST; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MAJOR CLINICAL STUDY; MIDDLE AGED; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SMAD GENE; STROMA; TGF BETA GENE; UPREGULATION; AGED; BREAST TUMOR; CANCER STAGING; GENETICS; METABOLISM; METASTASIS; MORTALITY; OUTCOME ASSESSMENT; PATHOLOGY; PROGNOSIS; RISK FACTOR; SIGNAL TRANSDUCTION; STROMA CELL;

ADULT; AGED; BREAST NEOPLASMS; CHEMOKINE CXCL1; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM METASTASIS; NEOPLASM STAGING; PATIENT OUTCOME ASSESSMENT; PROGNOSIS; PROTEIN BINDING; RISK FACTORS; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA; TUMOR MARKERS, BIOLOGICAL;

EID: 84929940887     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-781     Document Type: Article

References (87)

1. Desantis C, Ma J, Bryan L, Jemal A: Breast cancer statistics, 2013. CA Cancer J Clin 2013, 64:52-62.
2. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2013. CA Cancer J Clin 2013, 63(1):11-30.
3. Bombonati A, Sgroi DC: The molecular pathology of breast cancer progression. J Pathol 2011, 223(2):307-317.
4. Harkins B, Geyer CE Jr: Overcoming treatment challenges in advanced breast cancer. Semin Oncol Nurs 2007, 23(4 Suppl 2):S10-S16.
5. Amar S, Roy V, Perez EA: Treatment of metastatic breast cancer: looking towards the future. Breast Cancer Res Treat 2009, 114(3):413-422.
6. Koca E, Kuzan TY, Dizdar O, Babacan T, Sahin I, Ararat E, Altundag K: Outcomes of locally advanced breast cancer patients with >/= 10 positive axillary lymph nodes. Med Oncol 2013, 30(3):615.
7. Cheng YC, Ueno NT: Improvement of survival and prospect of cure in patients with metastatic breast cancer. Breast Cancer 2012, 19(3):191-199.
8. Hasebe T, Tsuda H, Tsubono Y, Imoto S, Mukai K: Fibrotic focus in invasive ductal carcinoma of the breast: a histopathological prognostic parameter for tumor recurrence and tumor death within three years after the initial operation. Jpn J Cancer Res 1997, 88(6):590-599.
9. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallet M, Park M: Stromal gene expression predicts clinical outcome in breast cancer. Nat Med 2008, 14(5):518-527.
10. Yamashita J, Ogawa M, Yamashita S, Nomura K, Kuramoto M, Saishoji T, Shin S: Immunoreactive hepatocyte growth factor is a strong and independent predictor of recurrence and survival in human breast cancer. Cancer Res 1994, 54(7):1630-1633.
11. Ahn S, Cho J, Sung J, Lee JE, Nam SJ, Kim KM, Cho EY: The prognostic significance of tumor-associated stroma in invasive breast carcinoma. Tumour Biol 2012, 33(5):1573-1580.
12. Wiseman BS, Werb Z: Stromal effects on mammary gland development and breast cancer. Science 2002, 296:1046-1049.
13. Polyak K, Kalluri R: The role of the microenvironment in mammary gland development and cancer. Cold Spring Harb Perspect Biol 2010, 2(11):a003244.
14. Ostman A, Augsten M: Cancer-associated fibroblasts and tumor growth-bystanders turning into key players. Curr Opin Genet Dev 2009, 19(1):67-73.
15. Polanska UM, Orimo A: Carcinoma-associated fibroblasts: non-neoplastic tumour-promoting mesenchymal cells. J Cell Physiol 2013, 228(8):1651-1657.
16. Hasebe T, Mukai K, Tsuda H, Ochiai A: New prognostic histological parameter of invasive ductal carcinoma of the breast: clinicopathological significance of fibrotic focus. Pathol Int 2000, 50(4):263-272.
17. Anastassiades OT, Pryce DM: Fibrosis as in indication of time in infiltrating breast cancer and its importance in prognosis. Br J Cancer 1974, 29(3):232-239.
18. Mezi S, Aloise G, Marzullo A, Marchei P, Di Benedetto A, Modica A, Vasaturo F, Modesti M: Prognostic significance of desmoplasia in breast carcinoma. A preliminary clinical study. Il Giornale di chirurgia 1997, 18(5):263-268.
19. Khramtsova G, Liao C, Khramtsov A, Li S, Gong C, Huo D, Nanda R: The M2/Alternative Activated Macrophage Phenotype Correlates with Aggressive Histopathologic features and Poor Clinical Outcome in Early Stage Breast Cancer. In Thirty-Second Annual CTRC-AACR San Antonio Breast Cancer Symposium-: 2009. San Antonio, TX: American Association for Cancer Research; 2009.
20. Hu M, Yao J, Carroll DK, Weremowicz S, Chen H, Carrasco D, Richardson A, Violette S, Nikolskaya T, Nikolsky Y, Bauerlein EL, Hhn WC, Gelman RS, Allred C, Bissel MJ, Schnitt S, Polyak K: Regulation of in situ to invasive breast carcinoma transition. Cancer Cell 2008, 13(5):394-406.
21. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA: 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.
22. Sadlonova A, Mukherjee S, Bowe DB, Gault SR, Dumas NA, Van Tine BA, Frolova N, Page GP, Welch DR, Novak L, Frost AR: Human breast fibroblasts inhibit growth of the MCF10AT xenograft model of proliferative breast disease. Am J Pathol 2007, 170(3):1064-1076.
23. Goss P, Parsons PG: The effect of hyperthermia and melphalan on survival of human fibroblast strains and melanoma cell lines. Cancer Res 1977, 37(1):152-156.
24. Lotti F, Jarrar AM, Pai RK, Hitomi M, Lathia J, Mace A, Gantt GA Jr, Sukhdeo K, Devecchio J, Vasanji A, Leahy P, Hjelmeland AB, Kalady MF, Rich JN: Chemotherapy activates cancer-associated fibroblasts to maintain colorectal cancer-initiating cells by IL-17A. J Exp Med 2013, 210(13:2851-2872.
25. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, True L, Nelson PS: Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 2012, 18(9):1359-1368.
26. Loeffler M, Kruger JA, Niethammer AG, Reisfeld RA: Targeting tumor-associated fibroblasts improves cancer chemotherapy by increasing intratumoral drug uptake. J Clin Invest 2006, 116(7):1955-1962.
27. Brennen WN, Rosen DM, Wang H, Isaacs JT, Denmeade SR: Targeting carcinoma-associated fibroblasts within the tumor stroma with a fibroblast activation protein-activated prodrug. J Natl Cancer Inst 2012, 104(17):1320-1334.
28. Narra K, Mullins SR, Lee HO, Strzemkowski-Brun B, Magalong K, Christiansen VJ, McKee PA, Egleston B, Cohen SJ, Weiner LM, Meropol NJ, Cheng JD: Phase II trial of single agent Val-boroPro (Talabostat) inhibiting Fibroblast Activation Protein in patients with metastatic colorectal cancer. Cancer Biol Ther 2007, 6(11):1691-1699.
29. Hofheinz RD, Al-Batran SE, Hartmann F, Hartung G, Jager D, Renner C, Tanswell P, Kunz U, Amelsberg A, Kuthan H, Stehle G: Stromal antigen targeting by a humanised monoclonal antibody: an early phase II trial of sibrotuzumab in patients with metastatic colorectal cancer. Onkologie 2003, 26(1):44-48.
30. Chen J, Li H, SundarRaj N, Wang JH: Alpha-smooth muscle actin expression enhances cell traction force. Cell Motil Cytoskeleton 2007, 64(4):248-257.
31. Ronnov-Jessen L, Petersen O: Induction of alpha-smooth muscle actin by transforming factor-beta 1 in quiescent human breast gland fibroblasts. Implication for myofibroblast generation in breast neoplasia. Lab Invest 1993, 68(6):696-707.
32. Sugimoto H, Mundel TM, Kieran MW, Kalluri R: Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol Ther 2006, 5(12):1640-1646.
33. Balkwill FR: The chemokine system and cancer. J Pathol 2012, 226(2):148-157.
34. White GE, Iqbal AJ, Greaves DR: CC chemokine receptors and chronic inflammation-therapeutic opportunities and pharmacological challenges. Pharmacol Rev 2013, 65(1):47-89.
35. Greaves NS, Ashcroft KJ, Baguneid M, Bayat A: Current understanding of molecular and cellular mechanisms in fibroplasia and angiogenesis during acute wound healing. J Dermatol Sci 2013, 72(3):206-217.
36. Strieter RM, Belperio JA, Burdick MD, Keane MP: CXC chemokines in angiogenesis relevant to chronic fibroproliferation. Curr Drug Targets Inflamm Allergy 2005, 4(1):23-26.
37. Stillie R, Farooq SM, Gordon JR, Stadnyk AW: The functional significance behind expressing two IL-8 receptor types on PMN. J Leukoc Biol 2009, 86(3):529-543.
38. Karagiannis GS, Saraon P, Jarvi KA, Diamandis EP: Proteomic signatures of angiogenesis in androgen-independent prostate cancer. Prostate 2014, 74(3):260-272.
39. Zhou SL, Dai Z, Zhou ZJ, Chen Q, Wang Z, Xiao YS, Hu ZQ, Huang XY, Yang GH, Shi YH, Qiu SJ, Fan J, Zhou J: CXCL5 contributes to tumor metastasis and recurrence of intrahepatic cholangiocarcinoma by recruiting infiltrative intratumoral neutrophils. Carcinogenesis 2014, 35:597-605.
40. Dhawan P, Richmond A: A novel NF-kappa B-inducing kinase-MAPK signaling pathway up-regulates NF-kappa B activity in melanoma cells. J Biol Chem 2002, 277(10):7920-7928.
41. Payne AS, Cornelius LA: The role of chemokines in melanoma tumor growth and metastasis. J Invest Dermatol 2002, 118(6):915-922.
42. Li J, Sidell N: Growth-related oncogene produced in human breast cancer cells and regulated by Syk protein-tyrosine kinase. Int J Cancer 2005, 117(1):14-20.
43. Vazquez-Martin A, Colomer R, Menendez JA: Protein array technology to detect HER2 (erbB-2)-induced 'cytokine signature' in breast cancer. Eur J Cancer 2007, 43(7):1117-1124.
44. Divella R, Daniele A, Savino E, Palma F, Bellizzi A, Giotta F, Simone G, Lioce M, Quaranta M, Paradiso A, Mazzocca AL: Circulating levels of transforming growth factor-beta (TGF-beta) and chemokine (C-X-C motif) ligand-1 (CXCL1) as predictors of distant seeding of circulating tumor cells in patients with metastatic breast cancer. Anticancer Res 2013, 33(4):1491-1497.
45. Bieche I, Chavey C, Andrieu C, Busson M, Vacher S, Le Corre L, Guinebretiere JM, Burlinchon S, Lidereau R, Lazennec G: CXC chemokines located in the 4q21 region are up-regulated in breast cancer. Endocr Relat Cancer 2007, 14(4):1039-1052.
46. Fujimoto H, Sangai T, Ishii G, Ikehara A, Nagashima T, Miyazaki M, Ochiai A: Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression. Int J Cancer 2009, 125(6):1276-1284.
47. Linder N, Konsti J, Turkki R, Rahtu E, Lundin M, Nordling S, Haglund C, Ahonen T, Pietikainen M, Lundin J: Identification of tumor epithelium and stroma in tissue microarrays using texture analysis. Diagn Pathol 2012, 7:22.
48. Lehr HA, van der Loos CM, Teeling P, Gown AM: Complete chromogen separation and analysis in double immunohistochemical stains using Photoshop-based image analysis. J Histochem Cytochem 1999, 47(1):119-126.
49. Chen J, Hicks D, Brantley-Sieders D, Cheng N, McCollum GW, Qi-Werdich X, Penn J: Inhibition of retinal neovascularization by soluble EphA2 receptor. Exp Eye Res 2006, 82(4):664-673.
50. Finak G, Sadekova S, Pepin F, Hallett M, Meterissian S, Halwani F, Khetani K, Souleimanova M, Zabolotny B, Omeroglu A, Park M: Gene expression signatures of morphologically normal breast tissue identify basal-like tumors. Breast Cancer Res 2006, 8(5):R58.
51. Guy C, Cardiff R, Muller W: Induction of mammary tumors by expression a polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992, 12:954-961.
52. Medina D, Kittrell F: In Methods in Mammary Gland Biology and Breast Cancer Research. edn. Edited by Ip MM, Asch BB. New York: Kluwer Academic/ Plenum Publishers; 2000:137-147.
53. Erbas B, Provenzano E, Armes J, Gertig D: The natural history of ductal carcinoma in situ of the breast: a review. Breast Cancer Res Treat 2006, 97(2):135-144.
54. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, Manova-Todorova K, Leversha M, Hogg N, Seshan VE, Sashan VE, Norton C, Boogi E, Massague J: A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012, 150(1):165-178.
55. Yerushalmi R, Hayes MM, Gelmon KA: Breast carcinoma-rare types: review of the literature. Ann Oncol 2009, 20(11):1763-1770.
56. Leonard GD, Swain SM: Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 2004, 96(12):906-920.
57. Cianfrocca M, Goldstein LJ: Prognostic and predictive factors in early-stage breast cancer. Oncologist 2004, 9(6):606-616.
58. Tsuchiya A, Abe R, Kanno M, Ohtake T, Fukushima T, Nomizu T, Kimijima I: Role of age as a prognostic factor in breast cancer. Surg Today 1997, 27(3):213-216.
59. Brewster AM, Hortobagyi GN, Broglio KR, Kau SW, Santa-Maria CA, Arun B, Buzdar AU, Booser DJ, Valero V, Bondy M, Esteva FJ: Residual risk of breast cancer recurrence 5 years after adjuvant therapy. J Natl Cancer Inst 2008, 100(16):1179-1183.
60. Schiavon G, Smith IE: Status of adjuvant endocrine therapy for breast cancer. Breast Cancer Res 2014, 16(2):206.
61. Brodmerkel CM, Huber R, Covington M, Diamond S, Hall L, Collins R, Leffet L, Gallagher K, Feldman P, Collier P, Stow M, Gu X, Baribaud F, Shin N, Thomas B, Burn T, Hollis G, Yeleswaram S, Solomon K, Friedman S, Wang A, Xue CB, Newton RC, Scherle P: Discovery and pharmacological characterization of a novel rodent-active CCR2 antagonist, INCB3344. J Immunol 2005, 175(8):5370-5378.
62. Pickup M, Novitskiy S, Moses HL: The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 2013, 13(11):788-799.
63. Moore-Smith L, Pasche B: TGFBR1 signaling and breast cancer. J Mammary Gland Biol Neoplasia 2011, 16(2):89-95.
64. Paraiso KH, Smalley KS: Fibroblast-mediated drug resistance in cancer. Biochem Pharmacol 2013, 85(8):1033-1041.
65. Virnig BA, Tuttle TM, Shamliyan T, Kane RL: Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes. J Natl Cancer Inst 2010, 102(3):170-178.
66. Ruder EH, Dorgan JF, Kranz S, Kris-Etherton PM, Hartman TJ: Examining breast cancer growth and lifestyle risk factors: early life, childhood, and adolescence. Clin Breast Cancer 2008, 8(4):334-342.
67. Gry M, Rimini R, Stromberg S, Asplund A, Ponten F, Uhlen M, Nilsson P: Correlations between RNA and protein expression profiles in 23 human cell lines. BMC Genomics 2009, 10:365.
68. Amiri KI, Richmond A: Fine tuning the transcriptional regulation of the CXCL1 chemokine. Prog Nucleic Acid Res Mol Biol 2003, 74:1-36.
69. Bachmeier BE, Mohrenz IV, Mirisola V, Schleicher E, Romeo F, Hohneke C, Jochum M, Nerlich AG, Pfeffer U: Curcumin downregulates the inflammatory cytokines CXCL1 and-2 in breast cancer cells via NFkappaB. Carcinogenesis 2008, 29(4):779-789.
70. Fan X, Chen X, DengW, Zhong G, Cai Q, Lin T: Up-regulated microRNA-143 in cancer stem cells differentiation promotes prostate cancer cells metastasis by modulating FNDC3B expression. BMC Cancer 2013, 13:61.
71. Yoo JK, Jung HY, Kim CH, Son WS, Kim JK: miR-7641 modulates the expression of CXCL1 during endothelial differentiation derived from human embryonic stem cells. Arch Pharm Res 2013, 36(3):353-358.
72. Pecot CV, Rupaimoole R, Yang D, Akbani R, Ivan C, Lu C, Wu S, Han HD, Shah MY, Rodriguez-Aguayo C, Bottsford-Miller J, Liu Y, Kim SB, Unruh A, Gonzalez-Villasana V, Huang L, Zand B, Moreno-Smith M, Mangala LS, Taylor M, Dalton HJ, Sehgal V, Wen Y, Kang Y, Baggerly KA, Lee JS, Ram PT, Ravoori MK, Kundra V, Zhang X, Ali-Fehmi R, Gonzalez-Angulo AM, Massion PP, Calin GA, Lopez-Berestein G, Zhang W, Sood AK: Tumour angiogenesis regulation by the miR-200 family. Nat Commun 2013, 4:2427.
73. Poluri KM, Joseph PR, Sawant KV, Rajarathnam K: Molecular basis of glycosaminoglycan heparin binding to the chemokine CXCL1 dimer. J Biol Chem 2013, 288(35):25143-25153.
74. Acosta JC, Gil J: A role for CXCR2 in senescence, but what about in cancer? Cancer Res 2009, 69(6):2167-2170.
75. Zaja-Milatovic S, Richmond A: CXC chemokines and their receptors: a case for a significant biological role in cutaneous wound healing. Histol Histopathol 2008, 23(11):1399-1407.
76. Gorska AE, Jensen RA, Shyr Y, Aakre ME, Bhowmick NA, Moses HL: Transgenic mice expressing a dominant-negative mutant type II transforming growth factor-beta receptor exhibit impaired mammary development and enhanced mammary tumor formation. Am J Pathol 2003, 163(4):1539-1549.
77. Bonine-Summers AR, Aakre ME, Brown KA, Arteaga CL, Pietenpol JA, Moses HL, Cheng N: Epidermal growth factor receptor plays a significant role in hepatocyte growth factor mediated biological responses in mammary epithelial cells. Cancer Biol Ther 2007, 6(4):561-570.
78. Fang WB, Jokar I, Chytil A, Moses HL, Abel T, Cheng N: Loss of one Tgfbr2 allele in fibroblasts promotes metastasis in MMTV: polyoma middle T transgenic and transplant mouse models of mammary tumor progression. Clin Exp Metastasis 2011, 28(4):351-366.
79. Mu L, Katsaros D, Lu L, Preti M, Durando A, Arisio R, Yu H: TGF-beta1 genotype and phenotype in breast cancer and their associations with IGFs and patient survival. Br J Cancer 2008, 99(8):1357-1363.
80. Figueroa JD, Flanders KC, Garcia-Closas M, Anderson WF, Yang XR, Matsuno RK, Duggan MA, Pfeiffer RM, Ooshima A, Cornelison R, Gierach GL, Brinton LA, Lissowska J, Peplonska B, Wakefield LM, Sherman ME: Expression of TGF-beta signaling factors in invasive breast cancers: relationships with age at diagnosis and tumor characteristics. Breast Cancer Res Treat 2010, 121(3):727-735.
81. de Kruijf EM, Dekker TJ, Hawinkels LJ, Putter H, Smit VT, Kroep JR, Kuppen PJ, van de Velde CJ, ten Dijke P, Tollenaar RA, Mesker WE: The prognostic role of TGF-beta signaling pathway in breast cancer patients. Ann Oncol 2013, 24(2):384-390.
82. Desruisseau S, Palmari J, Giusti C, Romain S, Martin PM, Berthois Y: Determination of TGFbeta1 protein level in human primary breast cancers and its relationship with survival. Br J Cancer 2006, 94(2):239-246.
83. Micke P, Ostman A: Exploring the tumour environment: cancer-associated fibroblasts as targets in cancer therapy. Expert Opin Ther Targets 2005, 9(6):1217-1233.
84. Berking C, Takemoto R, Schaider H, Showe L, Satyamoorthy K, Robbins P, Herlyn M: Transforming growth factor-beta1 increases survival of human melanoma through stroma remodeling. Cancer Res 2001, 61(22):8306-8316.
85. Kretzschmar M, Doody J, Timokhina I, Massague J: A mechanism of repression of TGFbeta/ Smad signaling by oncogenic Ras. Genes Dev 1999, 13(7):804-816.
86. Matsumura N, Huang Z, Mori S, Baba T, Fujii S, Konishi I, Iversen ES, Berchuck A, Murphy SK: Epigenetic suppression of the TGF-beta pathway revealed by transcriptome profiling in ovarian cancer. Genome Res 2011, 21(1):74-82.
87. Hinshelwood RA, Huschtscha LI, Melki J, Stirzaker C, Abdipranoto A, Vissel B, Ravasi T, Wells CA, Hume DA, Reddel RR, Clark SJ: Concordant epigenetic silencing of transforming growth factor-beta signaling pathway genes occurs early in breast carcinogenesis. Cancer Res 2007, 67(24):11517-11527.