Functions of chemokines in the perineural invasion of tumors (Review)

  • Authors:
    • Mei Zhang
    • Zhuo-Li Zhu
    • Xiao-Lei Gao
    • Jia-Shun Wu
    • Xin-Hua Liang
    • Ya-Ling Tang
  • View Affiliations

  • Published online on: March 8, 2018     https://doi.org/10.3892/ijo.2018.4311
  • Pages: 1369-1379
Metrics: HTML 0 views | PDF 0 views     Cited By (CrossRef): 0 citations

Abstract

The perineural invasion (PNI) of malignant tumors is a form of tumor progression in which cancer cells encroach along nerves. PNI hinders curative resection. Residual tumor cells in or around nerves can bring about local recurrence, infiltration and metastasis. This behavior is usually associated with a poor clinical prognosis. Therefore, it is necessary to investigate novel ligand-receptor crosstalk between nerves and tumor cells that promote the process of PNI. Chemokines are regarded as one of pivotal factors involved in the process of PNI. The present review collates information provided by previous studies with regard to the role of chemokines in PNI. The study presents a definition of PNI in cancer, generalizes the biological characteristics and the expression of chemokines and their receptors in cancer types associated with PNI, and discusses the underlying molecular mechanisms of chemokines, the reciprocal interactions between chemokines and other factors in PNI, and the interconnectivity of the microenvironment and chemokines. The aim of the review is to thoroughly illustrate the molecular cues of chemokines in cancer with PNI and to identify novel antitumor targets.

References

1 

Liebig C, Ayala G, Wilks JA, Berger DH and Albo D: Perineural invasion in cancer: A review of the literature. Cancer. 115:3379–3391. 2009. View Article : Google Scholar : PubMed/NCBI

2 

Lesnik DJ and Boey HP: Perineural invasion of the facial nerve by a cutaneous squamous cell cancer: A case report. Ear Nose Throat J 83. 824:826–827. 2004.

3 

Gupta A, Veness M, De'Ambrosis B, Selva D and Huilgol SC: Management of squamous cell and basal cell carcinomas of the head and neck with perineural invasion. Australas J Dermatol. 57:3–13. 2016. View Article : Google Scholar

4 

Pour PM, Bell RH and Batra SK: Neural invasion in the staging of pancreatic cancer. Pancreas. 26:322–325. 2003. View Article : Google Scholar : PubMed/NCBI

5 

Feng FY, Qian Y, Stenmark MH, Halverson S, Blas K, Vance S, Sandler HM and Hamstra DA: Perineural invasion predicts increased recurrence, metastasis, and death from prostate cancer following treatment with dose-escalated radiation therapy. Int J Radiat Oncol Biol Phys. 81:e361–e367. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Liebig C, Ayala G, Wilks J, Verstovsek G, Liu H, Agarwal N, Berger DH and Albo D: Perineural invasion is an independent predictor of outcome in colorectal cancer. J Clin Oncol. 27:5131–5137. 2009. View Article : Google Scholar : PubMed/NCBI

7 

Deng J, You Q, Gao Y, Yu Q, Zhao P, Zheng Y, Fang W, Xu N and Teng L: Prognostic value of perineural invasion in gastric cancer: A systematic review and meta-analysis. PLoS One. 9:e889072014. View Article : Google Scholar : PubMed/NCBI

8 

Zheng SC, Zhang YR, Luo SY and Zhang LP: The effect of GDNF on matrix-degrading and cell-adhesion during perineural invasion of salivary adenoid cystic carcinoma. Shanghai Kou Qiang Yi Xue. 25:212–216. 2016.In Chinese. PubMed/NCBI

9 

Figueira RC, Gomes LR, Neto JS, Silva FC, Silva ID and Sogayar MC: Correlation between MMPs and their inhibitors in breast cancer tumor tissue specimens and in cell lines with different metastatic potential. BMC Cancer. 9:202009. View Article : Google Scholar : PubMed/NCBI

10 

Batsakis JG: Nerves and neurotropic carcinomas. Ann Otol Rhinol Laryngol. 94:426–427. 1985.PubMed/NCBI

11 

Amit M, Na'ara S and Gil Z: Mechanisms of cancer dissemination along nerves. Nat Rev Cancer. 16:399–408. 2016. View Article : Google Scholar : PubMed/NCBI

12 

Abbadie C: Chemokines, chemokine receptors and pain. Trends Immunol. 26:529–534. 2005. View Article : Google Scholar : PubMed/NCBI

13 

Sommer C and Kress M: Recent findings on how proinflammatory cytokines cause pain: Peripheral mechanisms in inflammatory and neuropathic hyperalgesia. Neurosci Lett. 361:184–187. 2004. View Article : Google Scholar : PubMed/NCBI

14 

Charo IF and Ransohoff RM: The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med. 354:610–621. 2006. View Article : Google Scholar : PubMed/NCBI

15 

Griffith JW, Sokol CL and Luster AD: Chemokines and chemokine receptors: Positioning cells for host defense and immunity. Annu Rev Immunol. 32:659–702. 2014. View Article : Google Scholar : PubMed/NCBI

16 

Szekanecz Z, Vegvari A, Szabo Z and Koch AE: Chemokines and chemokine receptors in arthritis. Front Biosci (Schol Ed). 2:153–167. 2010. View Article : Google Scholar

17 

Gao YJ and Ji RR: Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther. 126:56–68. 2010. View Article : Google Scholar : PubMed/NCBI

18 

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

19 

Bonecchi R, Galliera E, Borroni EM, Corsi MM, Locati M and Mantovani A: Chemokines and chemokine receptors: An overview. Front Biosci (Landmark Ed). 14:540–551. 2009. View Article : Google Scholar

20 

Bryan SA, Jose PJ, Topping JR, Wilhelm R, Soderberg C, Kertesz D, Barnes PJ, Williams TJ, Hansel TT and Sabroe I: Responses of leukocytes to chemokines in whole blood and their antagonism by novel CC-chemokine receptor 3 antagonists. Am J Respir Crit Care Med. 165:1602–1609. 2002. View Article : Google Scholar : PubMed/NCBI

21 

Old EA and Malcangio M: Chemokine mediated neuron-glia communication and aberrant signalling in neuropathic pain states. Curr Opin Pharmacol. 12:67–73. 2012. View Article : Google Scholar

22 

Zlotnik A and Yoshie O: The chemokine superfamily revisited. Immunity. 36:705–716. 2012. View Article : Google Scholar : PubMed/NCBI

23 

Lefkowitz RJ: Seven transmembrane receptors: A brief personal retrospective. Biochim Biophys Acta. 1768:748–755. 2007. View Article : Google Scholar

24 

Hamm HE: The many faces of G protein signaling. J Biol Chem. 273:669–672. 1998. View Article : Google Scholar : PubMed/NCBI

25 

Violin JD and Lefkowitz RJ: Beta-arrestin-biased ligands at seven-transmembrane receptors. Trends Pharmacol Sci. 28:416–422. 2007. View Article : Google Scholar : PubMed/NCBI

26 

Curnock AP, Logan MK and Ward SG: Chemokine signalling: Pivoting around multiple phosphoinositide 3-kinases. Immunology. 105:125–136. 2002. View Article : Google Scholar : PubMed/NCBI

27 

DeWire SM, Ahn S, Lefkowitz RJ and Shenoy SK: Beta-arrestins and cell signaling. Annu Rev Physiol. 69:483–510. 2007. View Article : Google Scholar : PubMed/NCBI

28 

Logothetis DE, Kurachi Y, Galper J, Neer EJ and Clapham DE: The beta gamma subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature. 325:321–326. 1987. View Article : Google Scholar : PubMed/NCBI

29 

Wilson J and Balkwill F: The role of cytokines in the epithelial cancer microenvironment. Semin Cancer Biol. 12:113–120. 2002. View Article : Google Scholar : PubMed/NCBI

30 

Brew R, Erikson JS, West DC, Flanagan BF and Christmas SE: Interleukin-8 as a growth factor for human colorectal carcinoma cells in vitro. Biochem Soc Trans. 25:S2641997. View Article : Google Scholar

31 

Di Cesare S, Marshall JC, Logan P, Antecka E, Faingold D, Maloney SC and Burnier MN Jr: Expression and migratory analysis of 5 human uveal melanoma cell lines for CXCL12, CXCL8, CXCL1, and HGF. J Carcinog. 6:22007.PubMed/NCBI

32 

Liotta LA: An attractive force in metastasis. Nature. 410:24–25. 2001. View Article : Google Scholar : PubMed/NCBI

33 

Panda S, Padhiary SK and Routray S: Chemokines accentuating protumoral activities in oral cancer microenvironment possess an imperious stratagem for therapeutic resolutions. Oral Oncol. 60:8–17. 2016. View Article : Google Scholar : PubMed/NCBI

34 

Zhang S, Qi L, Li M, Zhang D, Xu S, Wang N and Sun B: Chemokine CXCL12 and its receptor CXCR4 expression are associated with perineural invasion of prostate cancer. J Exp Clin Cancer Res. 27:622008. View Article : Google Scholar : PubMed/NCBI

35 

He S, He S, Chen CH, Deborde S, Bakst RL, Chernichenko N, McNamara WF, Lee SY, Barajas F, Yu Z, et al: The chemokine (CCL2-CCR2) signaling axis mediates perineural invasion. Mol Cancer Res. 13:380–390. 2015. View Article : Google Scholar :

36 

Shen Z, Li T, Chen D, Jia S, Yang X, Liang L, Chai J, Cheng X, Yang X and Sun M: The CCL5/CCR5 axis contributes to the perineural invasion of human salivary adenoid cystic carcinoma. Oncol Rep. 31:800–806. 2014. View Article : Google Scholar

37 

Marchesi F, Piemonti L, Mantovani A and Allavena P: Molecular mechanisms of perineural invasion, a forgotten pathway of dissemination and metastasis. Cytokine Growth Factor Rev. 21:77–82. 2010. View Article : Google Scholar : PubMed/NCBI

38 

Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, et al: Involvement of chemokine receptors in breast cancer metastasis. Nature. 410:50–56. 2001. View Article : Google Scholar : PubMed/NCBI

39 

Dubový P, Klusáková I, Svízenská I and Brázda V: Spatio-temporal changes of SDF1 and its CXCR4 receptor in the dorsal root ganglia following unilateral sciatic nerve injury as a model of neuropathic pain. Histochem Cell Biol. 133:323–337. 2010. View Article : Google Scholar : PubMed/NCBI

40 

Hart CA, Brown M, Bagley S, Sharrard M and Clarke NW: Invasive characteristics of human prostatic epithelial cells: Understanding the metastatic process. Br J Cancer. 92:503–512. 2005. View Article : Google Scholar : PubMed/NCBI

41 

Schimanski CC, Bahre R, Gockel I, Müller A, Frerichs K, Hörner V, Teufel A, Simiantonaki N, Biesterfeld S, Wehler T, et al: Dissemination of hepatocellular carcinoma is mediated via chemokine receptor CXCR4. Br J Cancer. 95:210–217. 2006. View Article : Google Scholar : PubMed/NCBI

42 

Kollmar O, Rupertus K, Scheuer C, Junker B, Tilton B, Schilling MK and Menger MD: Stromal cell-derived factor-1 promotes cell migration and tumor growth of colorectal metastasis. Neoplasia. 9:862–870. 2007. View Article : Google Scholar : PubMed/NCBI

43 

Xu Q, Wang Z, Chen X, Duan W, Lei J, Zong L, Li X, Sheng L, Ma J, Han L, et al: Stromal-derived factor-1α/CXCL12-CXCR4 chemotactic pathway promotes perineural invasion in pancreatic cancer. Oncotarget. 6:4717–4732. 2015.PubMed/NCBI

44 

Kang H, Mansel RE and Jiang WG: Genetic manipulation of stromal cell-derived factor-1 attests the pivotal role of the autocrine SDF-1-CXCR4 pathway in the aggressiveness of breast cancer cells. Int J Oncol. 26:1429–1434. 2005.PubMed/NCBI

45 

Matteucci E, Locati M and Desiderio MA: Hepatocyte growth factor enhances CXCR4 expression favoring breast cancer cell invasiveness. Exp Cell Res. 310:176–185. 2005. View Article : Google Scholar : PubMed/NCBI

46 

Vaday GG, Hua SB, Peehl DM, Pauling MH, Lin YH, Zhu L, Lawrence DM, Foda HD and Zucker S: CXCR4 and CXCL12 (SDF-1) in prostate cancer: inhibitory effects of human single chain Fv antibodies. Clin Cancer Res. 10:5630–5639. 2004. View Article : Google Scholar : PubMed/NCBI

47 

Libura J, Drukala J, Majka M, Tomescu O, Navenot JM, Kucia M, Marquez L, Peiper SC, Barr FG, Janowska-Wieczorek A, et al: CXCR4-SDF-1 signaling is active in rhabdomyosarcoma cells and regulates locomotion, chemotaxis, and adhesion. Blood. 100:2597–2606. 2002. View Article : Google Scholar : PubMed/NCBI

48 

Esencay M, Newcomb EW and Zagzag D: HGF upregulates CXCR4 expression in gliomas via NF-kappaB: Implications for glioma cell migration. J Neurooncol. 99:33–40. 2010. View Article : Google Scholar : PubMed/NCBI

49 

Wu M, Chen Q, Li D, Li X, Li X, Huang C, Tang Y, Zhou Y, Wang D, Tang K, et al: LRRC4 inhibits human glioblastoma cells proliferation, invasion, and proMMP-2 activation by reducing SDF-1 alpha/CXCR4-mediated ERK1/2 and Akt signaling pathways. J Cell Biochem. 103:245–255. 2008. View Article : Google Scholar

50 

Roh J, Muelleman T, Tawfik O and Thomas SM: Perineural growth in head and neck squamous cell carcinoma: A review. Oral Oncol. 51:16–23. 2015. View Article : Google Scholar

51 

Zhang J, Sarkar S and Yong VW: The chemokine stromal cell derived factor-1 (CXCL12) promotes glioma invasiveness through MT2-matrix metalloproteinase. Carcinogenesis. 26:2069–2077. 2005. View Article : Google Scholar : PubMed/NCBI

52 

Zhu Y, Yang P, Zhang X, Zhang L, Cui G, Wang Q, Lv L, Zhang Y, Xin X, Yan T, et al: The effect and mechanism of CXCR4 silencing on metastasis suppression of human glioma U87 cell line. Anat Rec (Hoboken). 296:1857–1864. 2013. View Article : Google Scholar

53 

Marchesi F, Locatelli M, Solinas G, Erreni M, Allavena P and Mantovani A: Role of CX3CR1/CX3CL1 axis in primary and secondary involvement of the nervous system by cancer. J Neuroimmunol. 224:39–44. 2010. View Article : Google Scholar : PubMed/NCBI

54 

Bazan JF, Bacon KB, Hardiman G, Wang W, Soo K, Rossi D, Greaves DR, Zlotnik A and Schall TJ: A new class of membrane-bound chemokine with a CX3C motif. Nature. 385:640–644. 1997. View Article : Google Scholar : PubMed/NCBI

55 

Pan Y, Lloyd C, Zhou H, Dolich S, Deeds J, Gonzalo JA, Vath J, Gosselin M, Ma J, Dussault B, et al: Neurotactin, a membrane-anchored chemokine upregulated in brain inflammation. Nature. 387:611–617. 1997. View Article : Google Scholar : PubMed/NCBI

56 

Verge GM, Milligan ED, Maier SF, Watkins LR, Naeve GS and Foster AC: Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur J Neurosci. 20:1150–1160. 2004. View Article : Google Scholar : PubMed/NCBI

57 

Balkwill FR: Tumour necrosis factor and cancer. Prog Growth Factor Res. 4:121–137. 1992. View Article : Google Scholar : PubMed/NCBI

58 

Zeng Y, Jiang J, Huebener N, Wenkel J, Gaedicke G, Xiang R and Lode HN: Fractalkine gene therapy for neuroblastoma is more effective in combination with targeted IL-2. Cancer Lett. 228:187–193. 2005. View Article : Google Scholar : PubMed/NCBI

59 

Locatelli M, Boiocchi L, Ferrero S, Martinelli Boneschi F, Zavanone M, Pesce S, Allavena P, Maria Gaini S, Bello L and Mantovani A: Human glioma tumors express high levels of the chemokine receptor CX3CR1. Eur Cytokine Netw. 21:27–33. 2010.PubMed/NCBI

60 

Marchesi F, Piemonti L, Fedele G, Destro A, Roncalli M, Albarello L, Doglioni C, Anselmo A, Doni A, Bianchi P, et al: The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Cancer Res. 68:9060–9069. 2008. View Article : Google Scholar : PubMed/NCBI

61 

Andre F, Cabioglu N, Assi H, Sabourin JC, Delaloge S, Sahin A, Broglio K, Spano JP, Combadiere C, Bucana C, et al: Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer. Ann Oncol. 17:945–951. 2006. View Article : Google Scholar : PubMed/NCBI

62 

Shulby SA, Dolloff NG, Stearns ME, Meucci O and Fatatis A: CX3CR1-fractalkine expression regulates cellular mechanisms involved in adhesion, migration, and survival of human prostate cancer cells. Cancer Res. 64:4693–4698. 2004. View Article : Google Scholar : PubMed/NCBI

63 

Muller A, Sonkoly E, Eulert C, Gerber PA, Kubitza R, Schirlau K, Franken-Kunkel P, Poremba C, Snyderman C, Klotz LO, et al: Chemokine receptors in head and neck cancer: Association with metastatic spread and regulation during chemotherapy. Int J Cancer. 118:2147–2157. 2006. View Article : Google Scholar

64 

Fang WB, Jokar I, Zou A, Lambert D, Dendukuri P and Cheng N: CCL2/CCR2 chemokine signaling coordinates survival and motility of breast cancer cells through Smad3 protein- and p42/44 mitogen-activated protein kinase (MAPK)-dependent mechanisms. J Biol Chem. 287:36593–36608. 2012. View Article : Google Scholar : PubMed/NCBI

65 

Dagouassat M, Suffee N, Hlawaty H, Haddad O, Charni F, Laguillier C, Vassy R, Martin L, Schischmanoff PO, Gattegno L, et al: Monocyte chemoattractant protein-1 (MCP-1)/CCL2 secreted by hepatic myofibroblasts promotes migration and invasion of human hepatoma cells. Int J Cancer. 126:1095–1108. 2010.

66 

Vaday GG, Peehl DM, Kadam PA and Lawrence DM: Expression of CCL5 (RANTES) and CCR5 in prostate cancer. Prostate. 66:124–134. 2006. View Article : Google Scholar

67 

Borczuk AC, Papanikolaou N, Toonkel RL, Sole M, Gorenstein LA, Ginsburg ME, Sonett JR, Friedman RA and Powell CA: Lung adenocarcinoma invasion in TGFbetaRII-deficient cells is mediated by CCL5/RANTES. Oncogene. 27:557–564. 2008. View Article : Google Scholar

68 

Singh S, Singh R, Singh UP, Rai SN, Novakovic KR, Chung LW, Didier PJ, Grizzle WE and Lillard JW Jr: Clinical and biological significance of CXCR5 expressed by prostate cancer specimens and cell lines. Int J Cancer. 125:2288–2295. 2009. View Article : Google Scholar : PubMed/NCBI

69 

Qi XW, Xia SH, Yin Y, Jin LF, Pu Y, Hua D and Wu HR: Expression features of CXCR5 and its ligand, CXCL13 associated with poor prognosis of advanced colorectal cancer. Eur Rev Med Pharmacol Sci. 18:1916–1924. 2014.PubMed/NCBI

70 

El-Haibi CP, Singh R, Sharma PK, Singh S and Lillard JW Jr: CXCL13 mediates prostate cancer cell proliferation through JNK signalling and invasion through ERK activation. Cell Prolif. 44:311–319. 2011. View Article : Google Scholar : PubMed/NCBI

71 

Zhu Z, Zhang X, Guo H, Fu L, Pan G and Sun Y: CXCL13-CXCR5 axis promotes the growth and invasion of colon cancer cells via PI3K/AKT pathway. Mol Cell Biochem. 400:287–295. 2015. View Article : Google Scholar

72 

Kim HJ, Kim JS, Kang CD, Lee SJ, Kim JY, Yeon JE, Park JJ, Shim JJ, Byun KS, Bak YT, et al: Expression of epidermal growth factor receptor, ErbB2 and matrix metalloproteinase-9 in hepatolithiasis and cholangiocarcinoma. Korean J Gastroenterol. 45:52–59. 2005.In Korean. PubMed/NCBI

73 

Duan L, Hu XQ, Feng DY, Lei SY and Hu GH: GPC-1 may serve as a predictor of perineural invasion and a prognosticator of survival in pancreatic cancer. Asian J Surg. 36:7–12. 2013. View Article : Google Scholar

74 

Itatsu K, Sasaki M, Yamaguchi J, Ohira S, Ishikawa A, Ikeda H, Sato Y, Harada K, Zen Y, Sato H, et al: Cyclooxygenase-2 is involved in the up-regulation of matrix metalloproteinase-9 in cholangiocarcinoma induced by tumor necrosis factor-alpha. Am J Pathol. 174:829–841. 2009. View Article : Google Scholar : PubMed/NCBI

75 

Yang X, Dai J, Li T, Zhang P, Ma Q, Li Y, Zhou J and Lei D: Expression of EMMPRIN in adenoid cystic carcinoma of salivary glands: Correlation with tumor progression and patients' prognosis. Oral Oncol. 46:755–760. 2010. View Article : Google Scholar : PubMed/NCBI

76 

Yang X, Zhang P, Ma Q, Kong L, Li Y, Liu B and Lei D: EMMPRIN contributes to the in vitro invasion of human salivary adenoid cystic carcinoma cells. Oncol Rep. 27:1123–1127. 2012. View Article : Google Scholar

77 

Yang X, Zhang P, Ma Q, Kong L, Li Y, Liu B and Lei D: EMMPRIN silencing inhibits proliferation and perineural invasion of human salivary adenoid cystic carcinoma cells in vitro and in vivo. Cancer Biol Ther. 13:85–91. 2012. View Article : Google Scholar

78 

Anton ES, Weskamp G, Reichardt LF and Matthew WD: Nerve growth factor and its low-affinity receptor promote Schwann cell migration. Proc Natl Acad Sci USA. 91:2795–2799. 1994. View Article : Google Scholar

79 

Zhu Z, Kleeff J, Kayed H, Wang L, Korc M, Büchler MW and Friess H: Nerve growth factor and enhancement of proliferation, invasion, and tumorigenicity of pancreatic cancer cells. Mol Carcinog. 35:138–147. 2002. View Article : Google Scholar : PubMed/NCBI

80 

Zhu Z, Friess H, diMola FF, Zimmermann A, Graber HU, Korc M and Büchler MW: Nerve growth factor expression correlates with perineural invasion and pain in human pancreatic cancer. J Clin Oncol. 17:2419–2428. 1999. View Article : Google Scholar : PubMed/NCBI

81 

DeSchryver-Kecskemeti K, Balogh K and Neet KE: Nerve growth factor and the concept of neural-epithelial interactions. Immunohistochemical observations in two cases of vasitis nodosa and six cases of prostatic adenocarcinoma. Arch Pathol Lab Med. 111:833–835. 1987.PubMed/NCBI

82 

Okada Y, Eibl G, Duffy JP, Reber HA and Hines OJ: Glial cell-derived neurotrophic factor upregulates the expression and activation of matrix metalloproteinase-9 in human pancreatic cancer. Surgery. 134:293–299. 2003. View Article : Google Scholar : PubMed/NCBI

83 

Okada Y, Eibl G, Guha S, Duffy JP, Reber HA and Hines OJ: Nerve growth factor stimulates MMP-2 expression and activity and increases invasion by human pancreatic cancer cells. Clin Exp Metastasis. 21:285–292. 2004. View Article : Google Scholar : PubMed/NCBI

84 

Moscatelli I, Pierantozzi E, Camaioni A, Siracusa G and Campagnolo L: p75 neurotrophin receptor is involved in proliferation of undifferentiated mouse embryonic stem cells. Exp Cell Res. 315:3220–3232. 2009. View Article : Google Scholar : PubMed/NCBI

85 

Wang L, Sun M, Jiang Y, Yang L, Lei D, Lu C, Zhao Y, Zhang P, Yang Y and Li J: Nerve growth factor and tyrosine kinase A in human salivary adenoid cystic carcinoma: expression patterns and effects on in vitro invasive behavior. J Oral Maxillofac Surg. 64:636–641. 2006. View Article : Google Scholar : PubMed/NCBI

86 

Taylor S, Herrington S, Prime W, Rudland PS and Barraclough R: S100A4 (p9Ka) protein in colon carcinoma and liver metastases: Association with carcinoma cells and T-lymphocytes. Br J Cancer. 86:409–416. 2002. View Article : Google Scholar : PubMed/NCBI

87 

Jiang WG: E-cadherin and its associated protein catenins, cancer invasion and metastasis. Br J Surg. 83:437–446. 1996. View Article : Google Scholar : PubMed/NCBI

88 

Schmidt KN, Amstad P, Cerutti P and Baeuerle PA: Identification of hydrogen peroxide as the relevant messenger in the activation pathway of transcription factor NF-kappaB. Adv Exp Med Biol. 387:63–68. 1996. View Article : Google Scholar : PubMed/NCBI

89 

Wang CY, Mayo MW and Baldwin AS Jr: TNF- and cancer therapy-induced apoptosis: Potentiation by inhibition of NF-kappaB. Science. 274:784–787. 1996. View Article : Google Scholar : PubMed/NCBI

90 

Huang S, Pettaway CA, Uehara H, Bucana CD and Fidler IJ: Blockade of NF-kappaB activity in human prostate cancer cells is associated with suppression of angiogenesis, invasion, and metastasis. Oncogene. 20:4188–4197. 2001. View Article : Google Scholar : PubMed/NCBI

91 

Huang S, DeGuzman A, Bucana CD and Fidler IJ: Nuclear factor-kappaB activity correlates with growth, angiogenesis, and metastasis of human melanoma cells in nude mice. Clin Cancer Res. 6:2573–2581. 2000.PubMed/NCBI

92 

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

93 

Zheng Y, Miu Y, Yang X, Yang X and Zhu M: CCR7 Mediates TGF-β1-induced human malignant glioma invasion, migration, and epithelial-mesenchymal transition by activating MMP2/9 through the nuclear factor kappaB signaling pathway. DNA Cell Biol. 36:853–861. 2017. View Article : Google Scholar : PubMed/NCBI

94 

Zhong W, Tong Y, Li Y, Yuan J, Hu S, Hu T and Song G: Mesenchymal stem cells in inflammatory microenvironment potently promote metastatic growth of cholangiocarcinoma via activating Akt/NF-κB signaling by paracrine CCL5. Oncotarget. 8:73693–73704. 2017. View Article : Google Scholar : PubMed/NCBI

95 

Wang H, Cai J, Du S, Guo Z, Xin B, Wang J, Wei W and Shen X: Fractalkine/CX3CR1 induces apoptosis resistance and proliferation through the activation of the AKT/NF-κB cascade in pancreatic cancer cells. Cell Biochem Funct. 35:315–326. 2017. View Article : Google Scholar : PubMed/NCBI

96 

Anwar TE and Kleer CG: Tissue-based identification of stem cells and epithelial-to-mesenchymal transition in breast cancer. Hum Pathol. 44:1457–1464. 2013. View Article : Google Scholar : PubMed/NCBI

97 

Olmeda D, Montes A, Moreno-Bueno G, Flores JM, Portillo F and Cano A: Snai1 and Snai2 collaborate on tumor growth and metastasis properties of mouse skin carcinoma cell lines. Oncogene. 27:4690–4701. 2008. View Article : Google Scholar : PubMed/NCBI

98 

Carpenter RL, Paw I, Dewhirst MW and Lo HW: Akt phosphorylates and activates HSF-1 independent of heat shock, leading to Slug overexpression and epithelial-mesenchymal transition (EMT) of HER2-overexpressing breast cancer cells. Oncogene. 34:546–557. 2015. View Article : Google Scholar

99 

Hotz B, Arndt M, Dullat S, Bhargava S, Buhr HJ and Hotz HG: Epithelial to mesenchymal transition: Expression of the regulators snail, slug, and twist in pancreatic cancer. Clin Cancer Res. 13:4769–4776. 2007. View Article : Google Scholar : PubMed/NCBI

100 

Kalluri R and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest. 119:1420–1428. 2009. View Article : Google Scholar : PubMed/NCBI

101 

Thiery JP, Acloque H, Huang RY and Nieto MA: Epithelial-mesenchymal transitions in development and disease. Cell. 139:871–890. 2009. View Article : Google Scholar : PubMed/NCBI

102 

He Q, Zhou X, Li S, Jin Y, Chen Z, Chen D, Cai Y, Liu Z, Zhao T and Wang A: MicroRNA-181a suppresses salivary adenoid cystic carcinoma metastasis by targeting MAPK-Snai2 pathway. Biochim Biophys Acta. 1830:5258–5266. 2013. View Article : Google Scholar : PubMed/NCBI

103 

Chang B, Yang H, Jiao Y, Wang K, Liu Z, Wu P, Li S and Wang A: SOD2 deregulation enhances migration, invasion and has poor prognosis in salivary adenoid cystic carcinoma. Sci Rep. 6:259182016. View Article : Google Scholar : PubMed/NCBI

104 

Wang H, Liang X, Li M, Tao X, Tai S, Fan Z, Wang Z, Cheng B and Xia J: Chemokine (CC motif) ligand 18 upregulates Slug expression to promote stem-cell like features by activating the mammalian target of rapamycin pathway in oral squamous cell carcinoma. Cancer Sci. 108:1584–1593. 2017. View Article : Google Scholar : PubMed/NCBI

105 

Zhong G, Chen L, Yin R, Qu Y, Bao Y, Xiao Q, Zhang Z, Shen Y, Li C, Xu Y, et al: Chemokine (C-C motif) ligand 21/C-C chemokine receptor type 7 triggers migration and invasion of human lung cancer cells by epithelial-mesenchymal transition via the extracellular signal-regulated kinase signaling pathway. Mol Med Rep. 15:4100–4108. 2017. View Article : Google Scholar : PubMed/NCBI

106 

Li G, Yang Y, Xu S, Ma L, He M and Zhang Z: Slug signaling is up-regulated by CCL21/CCR7 [corrected] to induce EMT in human chondrosarcoma. Med Oncol. 32:4782015.

107 

Hou X, Zhang Y and Qiao H: CCL18 promotes the invasion and migration of gastric cancer cells via ERK1/2/NF-κB signaling pathway. Tumour Biol. 37:641–651. 2016. View Article : Google Scholar

108 

Zhao S, Wang J and Qin C: Blockade of CXCL12/CXCR4 signaling inhibits intrahepatic cholangiocarcinoma progression and metastasis via inactivation of canonical Wnt pathway. J Exp Clin Cancer Res. 33:1032014. View Article : Google Scholar : PubMed/NCBI

109 

Murre C, McCaw PS, Vaessin H, Caudy M, Jan LY, Jan YN, Cabrera CV, Buskin JN, Hauschka SD, Lassar AB, et al: Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 58:537–544. 1989. View Article : Google Scholar : PubMed/NCBI

110 

Ip YT, Park RE, Kosman D, Yazdanbakhsh K and Levine M: dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev. 6:1518–1530. 1992. View Article : Google Scholar : PubMed/NCBI

111 

Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A and Weinberg RA: Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 117:927–939. 2004. View Article : Google Scholar : PubMed/NCBI

112 

Kwok WK, Ling MT, Lee TW, Lau TC, Zhou C, Zhang X, Chua CW, Chan KW, Chan FL, Glackin C, et al: Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res. 65:5153–5162. 2005. View Article : Google Scholar : PubMed/NCBI

113 

Rosivatz E, Becker I, Specht K, Fricke E, Luber B, Busch R, Höfler H and Becker KF: Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol. 161:1881–1891. 2002. View Article : Google Scholar : PubMed/NCBI

114 

Wang D, Rai B, Qi F, Liu T, Wang J, Wang X and Ma B: Influence of the Twist gene on the invasion and metastasis of colon cancer. Oncol Rep. 39:31–44. 2018.

115 

Chen W, Gao Q, Han S, Pan F and Fan W: The CCL2/CCR2 axis enhances IL-6-induced epithelial-mesenchymal transition by cooperatively activating STAT3-Twist signaling. Tumour Biol. 36:973–981. 2015. View Article : Google Scholar

116 

Low-Marchelli JM, Ardi VC, Vizcarra EA, van Rooijen N, Quigley JP and Yang J: Twist1 induces CCL2 and recruits macrophages to promote angiogenesis. Cancer Res. 73:662–671. 2013. View Article : Google Scholar : PubMed/NCBI

117 

Xu C, Liu Y, Xiao L, Guo C, Deng S, Zheng S and Zeng E: The involvement of anterior gradient 2 in the stromal cell-derived factor 1-induced epithelial-mesenchymal transition of glioblastoma. Tumour Biol. 37:6091–6097. 2016. View Article : Google Scholar

118 

Koo YJ, Kim TJ, Min KJ, So KA, Jung US and Hong JH: CXCL11 mediates TWIST1-induced angiogenesis in epithelial ovarian cancer. Tumour Biol. 39:10104283177062262017. View Article : Google Scholar : PubMed/NCBI

119 

Li K, Xu B, Xu G and Liu R: CCR7 regulates Twist to induce the epithelial-mesenchymal transition in pancreatic ductal adenocarcinoma. Tumour Biol. 37:419–424. 2016. View Article : Google Scholar

120 

Franciszkiewicz K, Boissonnas A, Boutet M, Combadière C and Mami-Chouaib F: Role of chemokines and chemokine receptors in shaping the effector phase of the antitumor immune response. Cancer Res. 72:6325–6332. 2012. View Article : Google Scholar : PubMed/NCBI

121 

Wang D, Dubois RN and Richmond A: The role of chemokines in intestinal inflammation and cancer. Curr Opin Pharmacol. 9:688–696. 2009. View Article : Google Scholar : PubMed/NCBI

122 

Celesti G, Di Caro G, Bianchi P, Grizzi F, Marchesi F, Basso G, Rahal D, Delconte G, Catalano M, Cappello P, et al: Early expression of the fractalkine receptor CX3CR1 in pancreatic carcinogenesis. Br J Cancer. 109:2424–2433. 2013. View Article : Google Scholar : PubMed/NCBI

123 

Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, Bernasconi S, Saccani S, Nebuloni M, Vago L, et al: Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med. 198:1391–1402. 2003. View Article : Google Scholar : PubMed/NCBI

124 

Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP and Gurtner GC: Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 10:858–864. 2004. View Article : Google Scholar : PubMed/NCBI

125 

Rong Y, Durden DL, Van Meir EG and Brat DJ: 'Pseudopalisading' necrosis in glioblastoma: A familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis. J Neuropathol Exp Neurol. 65:529–539. 2006. View Article : Google Scholar : PubMed/NCBI

126 

Lin S, Wan S, Sun L, Hu J, Fang D, Zhao R, Yuan S and Zhang L: Chemokine C-C motif receptor 5 and C-C motif ligand 5 promote cancer cell migration under hypoxia. Cancer Sci. 103:904–912. 2012. View Article : Google Scholar : PubMed/NCBI

127 

Li Y, Qiu X, Zhang S, Zhang Q and Wang E: Hypoxia induced CCR7 expression via HIF-1alpha and HIF-2alpha correlates with migration and invasion in lung cancer cells. Cancer Biol Ther. 8:322–330. 2009. View Article : Google Scholar : PubMed/NCBI

128 

Zhao T, Gao S, Wang X, Liu J, Duan Y, Yuan Z, Sheng J, Li S, Wang F, Yu M, et al: Hypoxia-inducible factor-1α regulates chemotactic migration of pancreatic ductal adenocarcinoma cells through directly transactivating the CX3CR1 gene. PLoS One. 7:e433992012. View Article : Google Scholar

129 

Xiao LJ, Chen YY, Lin P, Zou HF, Lin F, Zhao LN, Li D, Guo L, Tang JB, Zheng XL, et al: Hypoxia increases CX3CR1 expression via HIF-1 and NF-κB in androgen-independent prostate cancer cells. Int J Oncol. 41:1827–1836. 2012. View Article : Google Scholar : PubMed/NCBI

130 

Trusolino L, Cavassa S, Angelini P, Andó M, Bertotti A, Comoglio PM and Boccaccio C: HGF/scatter factor selectively promotes cell invasion by increasing integrin avidity. FASEB J. 14:1629–1640. 2000. View Article : Google Scholar : PubMed/NCBI

131 

Matteucci E, Modora S, Simone M and Desiderio MA: Hepatocyte growth factor induces apoptosis through the extrinsic pathway in hepatoma cells: Favouring role of hypoxia-inducible factor-1 deficiency. Oncogene. 22:4062–4073. 2003. View Article : Google Scholar : PubMed/NCBI

132 

Zhang YW, Su Y, Volpert OV and Vande Woude GF: Hepatocyte growth factor/scatter factor mediates angiogenesis through positive VEGF and negative thrombospondin 1 regulation. Proc Natl Acad Sci USA. 100:12718–12723. 2003. View Article : Google Scholar : PubMed/NCBI

133 

Tacchini L, De Ponti C, Matteucci E, Follis R and Desiderio MA: Hepatocyte growth factor-activated NF-kappaB regulates HIF-1 activity and ODC expression, implicated in survival, differently in different carcinoma cell lines. Carcinogenesis. 25:2089–2100. 2004. View Article : Google Scholar : PubMed/NCBI

134 

Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer. 3:721–732. 2003. View Article : Google Scholar : PubMed/NCBI

135 

Niu G and Chen X: Vascular endothelial growth factor as an anti-angiogenic target for cancer therapy. Curr Drug Targets. 11:1000–1017. 2010. View Article : Google Scholar : PubMed/NCBI

136 

Owusu BY, Galemmo R, Janetka J and Klampfer L: Hepatocyte growth factor, a key tumor-promoting factor in the tumor microenvironment. Cancers (Basel). 9:92017. View Article : Google Scholar

Related Articles

Journal Cover

May 2018
Volume 52 Issue 5

Print ISSN: 1019-6439
Online ISSN:1791-2423

Sign up for eToc alerts

Recommend to Library

Copy and paste a formatted citation
APA
Zhang, M., Zhu, Z., Gao, X., Wu, J., Liang, X., & Tang, Y. (2018). Functions of chemokines in the perineural invasion of tumors (Review). International Journal of Oncology, 52, 1369-1379. https://doi.org/10.3892/ijo.2018.4311
MLA
Zhang, M., Zhu, Z., Gao, X., Wu, J., Liang, X., Tang, Y."Functions of chemokines in the perineural invasion of tumors (Review)". International Journal of Oncology 52.5 (2018): 1369-1379.
Chicago
Zhang, M., Zhu, Z., Gao, X., Wu, J., Liang, X., Tang, Y."Functions of chemokines in the perineural invasion of tumors (Review)". International Journal of Oncology 52, no. 5 (2018): 1369-1379. https://doi.org/10.3892/ijo.2018.4311