Mechanisms of CXCR7 induction in malignant melanoma development

Li,Xiao‑Jing; Liu,Pai; Tian,Wei‑Wei; Li,Zhi‑Feng; Liu,Bao‑Guo; Sun,Jian‑Fang

doi:10.3892/ol.2017.6720

Mechanisms of CXCR7 induction in malignant melanoma development

Authors:
- Xiao‑Jing Li
- Pai Liu
- Wei‑Wei Tian
- Zhi‑Feng Li
- Bao‑Guo Liu
- Jian‑Fang Sun
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Affiliations: Department of Dermatology, Affiliated Hospital of Hebei University of Engineering, Handan, Hebei 056002, P.R. China, Department of Dermatology, Jiangxi Province Dermatosis Special Hospital, Nanchang, Jiangxi 330000, P.R. China, Institute of Dermatology, Chinese Academy of Medical Sciences, Nanjing, Jiangsu 210042, P.R. China
Published online on: August 4, 2017 https://doi.org/10.3892/ol.2017.6720
Pages: 4106-4114
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Malignant melanoma (MM) is a highly malignant skin tumor. The mechanism of MM pathogenesis and its signaling pathways are not well characterized. C‑X‑C chemokine receptor type 7 (CXCR7) has been reported to regulate cancer cell invasion. The present study sought to investigate the effects of CXCR7 on MM development. First, CXCR7 expression levels were assessed in the skin tumor tissue of patients with MM. Then, CXCR7 small hairpin RNA was used in M14 melanoma cells in a Transwell culture model and in a transplanted mouse model to test the effects of CXCR7. In addition, immunohistochemistry staining, reverse transcription‑quantitative polymerase chain reaction and western blotting were used. The results revealed that CXCR7 expression levels were significantly higher in MM tissue compared with squamous cell carcinoma or basal cell carcinoma tissue. Knocking down CXCR7 in M14 cells significantly inhibited cell migration and invasion in the Transwell culture model. Furthermore, CXCR7 knockdown also significantly reduced the transplanted tumor size, weight and vascular number in the mouse model. It was concluded that CXCR7 interacts with C‑X‑C motif chemokine ligand 12 to activate the chemokine receptor signaling pathway, and to increase melanoma cell migration, invasion and development.

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1	Balch CM, Soong SJ, Gershenwald JE, Thompson JF, Reintgen DS, Cascinelli N, Urist M, McMasters KM, Ross MI, Kirkwood JM, et al: Prognostic factors analysis of 17,600 melanoma patients: Validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol. 19:3622–3634. 2001. View Article : Google Scholar : PubMed/NCBI
2	Balch CM, Soong SJ, Smith T, Ross MI, Urist MM, Karakousis CP, Temple WJ, Mihm MC, Barnhill RL, Jewell WR, et al: Long-term results of a prospective surgical trial comparing 2 cm vs. 4 cm excision margins for 740 patients with 1–4 mm melanomas. Ann Surg Oncol. 8:101–108. 2001. View Article : Google Scholar : PubMed/NCBI
3	Slominski A, Wortsman J, Carlson AJ, Matsuoka LY, Balch CM and Mihm MC: Malignant melanoma. Arch Pathol Lab Med. 125:1295–1306. 2001.PubMed/NCBI
4	Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, Fleming ID, Gershenwald JE, Houghton A Jr, Kirkwood JM, et al: Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol. 19:3635–3648. 2001. View Article : Google Scholar : PubMed/NCBI
5	DeSantis CE, Lin CC, Mariotto AB, Siegel RL, Stein KD, Kramer JL, Alteri R, Robbins AS and Jemal A: Cancer treatment and survivorship statistics, 2014. CA Cancer J Clin. 64:252–271. 2014. View Article : Google Scholar : PubMed/NCBI
6	Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, Foshag LJ and Cochran AJ: Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg. 127:392–399. 1992. View Article : Google Scholar : PubMed/NCBI
7	Baggiolini M and Loetscher P: Chemokines in inflammation and immunity. Immunol Today. 21:418–420. 2000. View Article : Google Scholar : PubMed/NCBI
8	Balkwill F: Cancer and the chemokine network. Nat Rev Cancer. 4:540–550. 2004. View Article : Google Scholar : PubMed/NCBI
9	Rossi D and Zlotnik A: The biology of chemokines and their receptors. Annu Rev Immunol. 18:217–242. 2000. View Article : Google Scholar : PubMed/NCBI
10	Sánchez-Martin L, Sánchez-Mateos P and Cabañas C: CXCR7 impact on CXCL12 biology and disease. Trends Mol Med. 19:12–22. 2013. View Article : Google Scholar : PubMed/NCBI
11	Beutner KR, Geisse JK, Helman D, Fox TL, Ginkel A and Owens ML: Therapeutic response of basal cell carcinoma to the immune response modifier imiquimod 5% cream. J Am Acad Dermatol. 41:1002–1007. 1999. View Article : Google Scholar : PubMed/NCBI
12	Rowe DE, Carroll RJ and Day CL Jr: Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. Implications for treatment modality selection. J Am Acad Dermatol. 26:976–990. 1992. View Article : Google Scholar : PubMed/NCBI
13	Shaw LM: Tumor cell invasion assays. Methods Mol Biol. 294:97–105. 2005.PubMed/NCBI
14	Yang FC, Atkinson SJ, Gu Y, Borneo JB, Roberts AW, Zheng Y, Pennington J and Williams DA: Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc Natl Acad Sci USA. 98:5614–5618. 2001. View Article : Google Scholar : PubMed/NCBI
15	Tsareva SA, Moriggl R, Corvinus FM, Wiederanders B, Schütz A, Kovacic B and Friedrich K: Signal transducer and activator of transcription 3 activation promotes invasive growth of colon carcinomas through matrix metalloproteinase induction. Neoplasia. 9:279–291. 2007. View Article : Google Scholar : PubMed/NCBI
16	Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, Dosik H and Parks WP: In vitro cultivation of human tumors: Establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst. 51:1417–1423. 1973. View Article : Google Scholar : PubMed/NCBI
17	Sulit HL, Golub SH, Irie RF, Gupta RK, Grooms GA and Morton DL: Human tumor cells grown in fetal calf serum and human serum: Influences on the tests for lymphocyte cytotoxicity, serum blocking and serum arming effects. Int J Cancer. 17:461–468. 1976. View Article : Google Scholar : PubMed/NCBI
18	Larionov A, Krause A and Miller W: A standard curve based method for relative real time PCR data processing. BMC Bioinformatics. 6:622005. View Article : Google Scholar : PubMed/NCBI
19	Sun X, Cheng G, Hao M, Zheng J, Zhou X, Zhang J, Taichman RS, Pienta KJ and Wang J: CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev. 29:709–722. 2010. View Article : Google Scholar : PubMed/NCBI
20	Wang J, Shiozawa Y, Wang J, Wang Y, Jung Y, Pienta KJ, Mehra R, Loberg R and Taichman RS: The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem. 283:4283–4294. 2008. View Article : Google Scholar : PubMed/NCBI
21	Huggenberger R and Detmar M: The cutaneous vascular system in chronic skin inflammation. J Investig Dermatol Symp Proc. 15:24–32. 2011. View Article : Google Scholar : PubMed/NCBI
22	Tarnowski M, Liu R, Wysoczynski M, Ratajczak J, Kucia M and Ratajczak MZ: CXCR7: A new SDF-1-binding receptor in contrast to normal CD34(+) progenitors is functional and is expressed at higher level in human malignant hematopoietic cells. Eur J Haematol. 85:472–483. 2010. View Article : Google Scholar : PubMed/NCBI
23	D'Alterio C, Consales C, Polimeno M, Franco R, Cindolo L, Portella L, Cioffi M, Calemma R, Marra L, Claudio L, et al: Concomitant CXCR4 and CXCR7 expression predicts poor prognosis in renal cancer. Curr Cancer Drug Targets. 10:772–781. 2010. View Article : Google Scholar : PubMed/NCBI
24	Pinto S, Martinez-Romero A, O'Connor JE, Gil-Benso R, San-Miguel T, Terrádez L, Monteagudo C and Callaghan RC: Intracellular coexpression of CXC- and CC-chemokine receptors and their ligands in human melanoma cell lines and dynamic variations after xenotransplantation. BMC Cancer. 14:1182014. View Article : Google Scholar : PubMed/NCBI
25	Richmond A, Yang J and Su Y: The good and the bad of chemokines/chemokine receptors in melanoma. Pigment Cell Melanoma Res. 22:175–186. 2009. View Article : Google Scholar : PubMed/NCBI
26	Longo-Imedio MI, Longo N, Treviño I, Lázaro P and Sánchez-Mateos P: Clinical significance of CXCR3 and CXCR4 expression in primary melanoma. Int J Cancer. 117:861–865. 2005. View Article : Google Scholar : PubMed/NCBI
27	Monteagudo C, Martin JM, Jorda E and Llombart-Bosch A: CXCR3 chemokine receptor immunoreactivity in primary cutaneous malignant melanoma: Correlation with clinicopathological prognostic factors. J Clin Pathol. 60:596–599. 2007. View Article : Google Scholar : PubMed/NCBI
28	Levoye A, Balabanian K, Baleux F, Bachelerie F and Lagane B: CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood. 113:6085–6093. 2009. View Article : Google Scholar : PubMed/NCBI
29	Lee E, Han J, Kim K, Choi H, Cho EG and Lee TR: CXCR7 mediates SDF1-induced melanocyte migration. Pigment Cell Melanoma Res. 26:58–66. 2013. View Article : Google Scholar : PubMed/NCBI
30	Sierro F, Biben C, Martinez-Muñoz L, Mellado M, Ransohoff RM, Li M, Woehl B, Leung H, Groom J, Batten M, et al: Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci USA. 104:14759–14764. 2007. View Article : Google Scholar : PubMed/NCBI
31	Salazar N, Muñoz D, Kallifatidis G, Singh RK, Jordà M and Lokeshwar BL: The chemokine receptor CXCR7 interacts with EGFR to promote breast cancer cell proliferation. Mol Cancer. 13:1982014. View Article : Google Scholar : PubMed/NCBI
32	Singh RK and Lokeshwar BL: The IL-8-regulated chemokine receptor CXCR7 stimulates EGFR signaling to promote prostate cancer growth. Cancer Res. 71:3268–3277. 2011. View Article : Google Scholar : PubMed/NCBI