Interaction of tumour cells with their microenvironment: Ion channels and cell adhesion molecules. A focus on pancreatic cancer

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1638, 2014, Pages

  Arcangeli, Annarosa ^a   Crociani, Olivia ^a   Bencini, Lapo ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b CAREGGI UNIVERSITY HOSPITAL   (Italy)

Author keywords

Cell signalling; Desmoplastic reaction; Integrins; Ion channels; Pancreatic cancer; Tumour microenvironment

Indexed keywords

BIOCHEMISTRY; CANCER; CYTOLOGY; DISEASE TREATMENT; GROWTH RESPONSE; ION; PATHOLOGY; PHYSIOLOGY; PROTEIN; SIGNALING; TUMOR;

INTEGRIN; ION CHANNEL;

BIOLOGICAL MODEL; CELL ADHESION; CELL SIGNALLING; DESMOPLASTIC REACTION; HUMAN; METABOLISM; PANCREAS CANCER; PANCREAS TUMOR; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

CELL SIGNALLING; DESMOPLASTIC REACTION; INTEGRINS; ION CHANNELS; PANCREATIC CANCER; TUMOUR MICROENVIRONMENT;

CELL ADHESION; HUMANS; INTEGRINS; ION CHANNELS; MODELS, BIOLOGICAL; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84893465773     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0101     Document Type: Review

References (95)

1. Comoglio PM, Trusolino L. 2005 Cancer: the matrix is now in control. Nat. Med. 11, 1156-1159. (doi:10.1038/nm1105-1156)
2. Girieca L, Ruegg C. 2008 The tumor microenvironment and its contribution to tumor evolution toward metastasis. Histochem. Cell Biol. 130, 1091-1103. (doi:10.1007/s00418-008-0530-8)
3. Joyce JA, Pollard JW. 2009 Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252. (doi:10.1038/nrc2618)
4. Nwajei F, Konopleva M. 2013 The bone marrow microenvironment as niche retreats for hematopoietic and leukemic stem cells. Adv. Hematol. 2013, 8. (doi:10.1155/2013/953982)
5. Mahadevan D, Von Hoff DD. 2007 Tumor-stroma interactions in pancreatic ductal denocarcinoma. Mol. Cancer Ther. 6, 1186-1197. (doi:10.1158/1535-7163.MCT-06-0686)
6. Li X, Ma Q, Xu Q, Duan W, Lei J, Wu E. 2012 Targeting the cancer-stroma interaction: a potential approach for pancreatic cancer treatment. Curr. Pharm. Des. 18, 2404-2415. (doi:10.2174/13816128112092404)
7. Cruickshank AH. 1986 Pathology of the pancreas. Berlin and Heidelberg, Germany: Springer-Verlag.
8. Hanahan D, Weimberg RA. 2011 Hallmarks of cancer: the next generation. Cell 144, 646-674. (doi:10.1016/j.cell.2011.02.013)
9. Ruoslahti E, Bhatia SN, Sailor MJ. 2010 Targeting of drugs and nanoparticles to tumors. J. Cell Biol. 188, 759-768. (doi:10.1083/jcb.200910104)
10. Arcangeli A, Crociani O, Lastraioli E, Masi A, Pillozzi S, Becchetti A. 2009 Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr. Med. Chem. 16, 66-93. (doi:10.2174/092986709787002835)
11. Arcangeli A. 2011 Ion channels and transporters in cancer. 3. Ion channels in the tumor cellmicroenvironment cross talk. Am. J. Physiol. Cell. Physiol. 301, C762-C771. (doi:10.1152/ajpcell. 00113.2011)
12. Fiorio Pla A, Avanzato D, Munaron L, Ambudkar IS. 2012 Ion channels and transporters in cancer. 6. Vascularizing the tumor: TRP channels as molecular targets. Am. J. Physiol. Cell Physiol. 302, C9-C15. (doi:10.1152/ajpcell.00280.2011)
13. ATP channels in mesenchymal stromal stem cells: strong upregulation of Kir6.2 subunits upon osteogenic differentiation. Tissue Cell 43, 331-336. (doi:10.1016/j.tice.2011.06.004)
14. Pillozzi S, Becchetti A. 2012 Ion channels in hematopoietic and mesenchymal stem cells. Stem Cells Int. 2012, 9. (doi:10.1155/2012/217910)
15. + channels in human T lymphocytes: a role in mitogenesis? Nature 307, 465-468. (doi:10.1038/307465a0)
16. Cahalan MD, Chandy KG. 2009 The functional network of ion channels in T lymphocytes. Immunol. Rev. 231, 59-87. (doi:10.1111/j.1600-065X.2009.00816.x)
17. Feske S, Skolnik EY, Prakriya M. 2012 Ion channels and transporters in lymphocyte function and immunity. Nat. Rev. Immunol. 12, 532-547. (doi:10.1038/nri3233)
18. Prevarskaya N, Skryma R, Shuba Y. 2010 Ion channels and the hallmarks of cancer. Trends Mol. Med. 16, 107-121. (doi:10.1016/j.molmed.2010. 01.005)
19. Beech DJ. 2012 Orai1 calcium channels in the vasculature. Pflugers Arch. 463, 635-647. (doi:10.1007/s00424-012-1090-2)
20. Nagy JA, Chang SH, Shih SC, Dvorak AM, Dvorak HF. 2010 Heterogeneity of the tumor vasculature. Semin. Thromb. Hemost. 36, 321-331. (doi:10.1055/s-0030-1253454)
21. Kalluri R, Zeisberg M. 2006 Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401. (doi:10.1038/nrc1877)
22. Farrow B, Rowley D, Dang T, Berger DH. 2009 Characterization of tumor derived pancreatic stellate cells. J. Surg. Res. 157, 96-102. (doi:10.1016/j.jss. 2009.03.064)
23. Sato N, Maehara N, Goggins M. 2004 Gene expression profiling of tumor stromal interactions between pancreatic cancer cells and stromal fibroblasts. Cancer Res. 64, 6950-6956. (doi:10.1158/0008-5472.CAN-04-0677)
24. Bhowmick NA, Moses HL. 2005 Tumor-stroma interactions. Curr. Opin. Genet. Dev. 15, 97-101. (doi:10.1016/j.gde.2004.12.00)
25. Bindea G, Mlecnik B, Fridman WH, Page's F, Galon J. 2010 Natural immunity to cancer in humans. Curr. Opin. Immunol. 22, 215-222. (doi:10.1016/j.coi. 2010.02.006)
26. Johansson M, Denardo DG, Coussens LM. 2008 Polarized immune responses differentially regulate cancer development. Immunol. Rev. 222, 145-154. (doi:10.1111/j.1600-065X.2008.00600.x)
27. Becchetti A, Pillozzi S, Morini R, Nesti E, Arcangeli A. 2010 New insights into the regulation of ion channels by integrins. Int. Rev. Cell. Mol. Biol. 279, 135-190. (doi:10.1016/S1937-6448(10)79005-5)
28. + channels. Adv. Exp. Med. Biol. 674, 81-94. (doi:10.1007/978-1-4419-6066-5_8)
29. Lopez-Castejon G, Theaker J, Pelegrin P, Clifton AD, Braddock M, Surprenant A. 2010 P2X7 Receptormediated release of cathepsins from macrophages is a cytokine-independent mechanism potentially involved in joint diseases. J. Immunol. 185, 2611-2619. (doi:10.4049/jimmunol.1000436)
30. Barkan D, Green JE, Chambers AF. 2010 Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur. J. Cancer 46, 1181-1188. (doi:10.1016/j.ejca.2010.02.027)
31. Kessenbrock K, Plaks V, Werb Z. 2010 Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141, 52-67. (doi:10.1016/j. cell.2010.03.015)
32. Ferrara N, Gerber HP, LeCouter J. 2003 The biology of VEGF and its receptors. Nat. Med. 9, 669-676. (doi:10.1038/nm0603-669)
33. Hynes RO. 2002 Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687. (doi:10.1016/S0092-8674(02)00971-6)
34. de Pereda JM, Wiche G, Liddington RC. 1999 Crystal structure of a tandem pair of fibronectin type III domains from the cytoplasmic tail of integrin alpha6beta4. EMBO J. 18, 4087-4095. (doi:10.1093/emboj/18.15.4087)
35. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM, Ginsberg MH, Calderwood DA. 2003 Talin binding to integrin beta tails: a final common step in integrin activation. Science 302, 103-106. (doi:10.1126/science.1086652)
36. Ginsberg MH, Partridge A, Shattil SJ. 2005 Integrin regulation. Curr. Opin. Cell Biol. 17, 509-516. (doi:10.1016/j.ceb.2005.08.010)
37. Miranti CK, Brugge JS. 2002 Sensing the environment. A historical perspective of integrin signal transduction. Nat. Cell Biol. 4, E83-E90. (doi:10.1038/ncb0402-e83)
38. Cabodi S et al. 2010 Integrins and signal transduction. Adv. Exp. Med. Biol. 674, 43-54. (doi:10.1007/978-1-4419-6066-5_5)
39. Arcangeli A, Becchetti A. 2006 Complex functional interaction between integrin receptors and ion channels. Trends Cell Biol. 16, 631-639. (doi:10.1016/j.tcb.2006.10.003)
40. Arcangeli A et al. 1993 Integrin mediated neurite outgrowth in neuroblastoma cells depends on the activation of potassium channels. J. Cell Biol. 122, 1131-1143. (doi:10.1083/jcb.122.5.1131)
41. + current. Proc. R. Soc. Lond. B 248, 235-240. (doi:10.1098/rspb.1992.0067)
42. 2+ channels. Cell 67, 21-33. (doi:10.1016/0092-8674(91)90569-K)
43. + channels activation during β1 integrin-mediated adhesion to fibronectin induces an up-regulation of αvβ3 integrin in the preosteoclastic leukemia cell line FLG 29.1. J. Biol. Chem. 276, 4923-4931. (doi:10.1074/jbc.M005682200)
44. +-ATPase activity influence cell attachment to fibronectin. Am. J. Physiol. Cell Physiol. 282, C302-C309. (doi:10.1152/ajpcell. 00117.2001)
45. Menegazzi R, Busetto S, Cramer R, Dri P, Patriarca P. 2000 Role of intracellular chloride in the reversible activation of neutrophil b2 integrins: a lesson from TNF stimulation. J. Immunol. 165, 4606-4614. (doi:10.1016/j.bcmd.2009.01.006)
46. Tominaga T, Barber DL. 1998 Na-H exchange acts downstream of RhoA to regulate integrin-induced cell adhesion and spreading. Mol. Biol. Cell 9, 2287-2303. (doi:10.1091/mbc.9.8.2287)
47. + exchanger in metastasis. Nat. Rev. Cancer 5, 786-795. (doi:10.1038/nrc1713)
48. Davis MJ, Wu X, Nurkiewicz TR, Kawasaki J, Gui P, Hill MA, Wilson E. 2002 Regulation of ion channels by integrins. Cell Biochem. Biophys. 36, 41-66. (doi:10.1385/CBB:36:1:41)
49. Katsumi A, Orr AW, Tzima E, Schwartz MA. 2004 Integrins in mechanotransduction. J. Biol. Chem. 279, 12 001-12 004. (doi:10.1074/jbc. R300038200)
50. + and opening of voltage gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and β1 integrins. J. Exp. Med. 191, 1167-1176. (doi:10.1084/jem.191.7.1167)
51. 1-integrins on the plasma membrane of melanoma cells: effects of cell adherence and channel blockers. J. Gen. Physiol. 120, 29-37. (doi:10.1085/jgp.20028607)
52. + channels and β1 integrins interact through the assembly of a macromolecular complex. Ann. NY Acad. Sci. 973, 559-561. (doi:10.1111/j.1749-6632.2002.tb04701.x)
53. Cherubini A et al. 2005 hERG1 channels are physically linked to beta1 integrins and modulate adhesion-dependent signalling. Mol. Biol. Cell 16, 2972-2983. (doi:10.1091/mbc.E04-10-0940)
54. + channel form a macromolecular signaling complex in acute myeloid leukemia: role in cell migration and clinical outcome. Blood 110, 1238-1250. (doi:10.1182/blood-2006-02-003772)
55. Pillozzi S et al. 2011 Chemotherapy resistance in acute lymphoblastic leukemia requires hERG1 channels and is overcome by hERG1 blockers. Blood 117, 902-914. (doi:10.1182/blood-2010-01-262691)
56. Crociani O et al. 2013 hERG1 channels modulate integrin signaling to trigger angiogenesis and tumor progression in colorectal cancer. Sci. Rep. (doi:10.1038/srep03188)
57. Dozynkiewicz MA et al. 2012 Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev. Cell 22, 131-145. (doi:10.1016/j.devcel.2011. 11.008)
58. Schwab A, Nechyporuk-Zloy V, Fabian A, Stock C. 2007 Cells move when ions and water flow. Pflugers Arch. 453, 421-432. (doi:10.1007/s00424-006-0138-6)
59. Nechyporuk-Zloy V, Dieterich P, Oberleithner H, Stock C, Schwab A. 2008 Dynamics of single potassium channel proteins in the plasma membrane of migrating cells. Am. J. Physiol. Cell Physiol. 294, C1096-1102. (doi:10.1152/ajpcell. 00252.2007)
60. Rezzonico R et al. 2003 Focal adhesion kinase pp125FAK interacts with the large conductance calcium-activated hSlo potassium channel in human osteoblasts: potential role in mechanotransduction. J. Bone Miner. Res. 18, 1863-1871. (doi:10.1359/jbmr.2003.18.10.1863)
61. Wei JF et al. 2008 Formation of Kv2.1-FAK complex as a mechanism of FAK activation, cell polarization and enhanced motility. J. Cell Physiol. 217, 544-557. (doi:10.1002/jcp.21530)
62. Tian L, Chen L, McClafferty H, Sailer CA, Ruth P, Knaus HG, Shipston MJ. 2006 A noncanonical SH3 domain binding motif links BK channels to the actin cytoskeleton via the SH3 adapter cortactin. FASEB J. 20, 2588-2590. (doi:10.1096/fj.06-6152fje)
63. Williams MR, Markey JC, Doczi MA, Morielli AD. 2007 An essential role for cortactin in the modulation of the potassium channel Kv1.2. Proc. Natl Acad. Sci. USA 104, 17 412-17 417. (doi:10.1073/pnas.0703865104)
64. de Hart GW, Jin T, McCloskey DE, Pegg AE, Sheppard D. 2008 The α9β1 integrin enhances cell migration by polyamine-mediated modulation of an inward-rectifier potassium channel. Proc. Natl Acad. Sci. USA 105, 7188-7193. (doi:10.1073/pnas. 0708044105)
65. Vandenberg CA. 2008 Integrins step up the pace of cell migration through polyamines and potassium channels. Proc. Natl Acad. Sci. USA 105, 7109-7110. (doi:10.1073/pnas.0803231105)
66. 2 integrins: relationship with spreading and activation of the respiratory burst. J. Immunol. 162, 423-434.
67. 4 integrin and calcium activated chloride channels (CLCAs) in metastasis. J. Biol. Chem. 278, 49 406-49 416. (doi:10.1074/jbc. M309086200)
68. Leavesley DI, Schwartz MA, Rosenfeld M, Cheresh DA. 1993 Integrin β-1 and β-3-mediated endothelial cell migration is triggered through distinct signaling mechanisms. J. Cell Biol. 121, 163-170. (doi:10.1083/jcb.121.1.163)
69. Brenner H et al. 2009 Long-term survival expectations of cancer patients in Europe in 2000-2002. Eur. J. Cancer 45, 1028-1041. (doi:10.1016/j.ejca.2008.11.005)
70. Yang GY, Wagner TD, Fuss M, Thomas CR. 2005 Multimodality approaches for pancreatic cancer. Cancer J. Clin. 55, 352-367. (doi:10.3322/canjclin. 55.6.352)
71. Hochster HS, Haller DG, de Gramont A, Berlin JD, Philip PA, Moore MJ, Ajani JA. 2006 Consensus report of the international society of gastrointestinal oncology on therapeutic prograss in advanced pancreatic cancer. Cancer 107, 676-685. (doi:10.1002/cncr.22036)
72. Zuckerman DS, Ryan DP. 2008 Adjuvant therapy for pancreatic cancer. Cancer 112, 243-249. (doi:10.1002/cncr.23174)
73. Rivera F, López-Tarruella S, Vega-Villegas ME, Salcedo M. 2009 Treatment of advanced pancreatic cancer: from gemcitabine single agent to combinations and targeted therapy. Cancer Treat. Rev. 35, 335-339. (doi:10.1016/j.ctrv.2008.11.007)
74. El Maalouf G, Le Tourneau C, Batty GN, Faivre S, Raymond E. 2009 Markers involved in resistance to cytotoxics and targeted therapeutics in pancreatic cancer. Cancer Treat. Rev. 35, 167-174. (doi:10.1016/j.ctrv.2008.10.002)
75. Cunha GR. 1994 Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate. Cancer 74, 1030-1044. (doi:10.1002/1097-0142(19940801)74:3+,1030::AIDCNCR2820741510.3.0. CO;2-Q)
76. Li Z, Manna P, Kobayashi H, Spilde T, Bhatia A, Preuett B, Prasadan K, Hembree M, Gittes GK. 2004 Multifaceted pancreatic mesenchymal control of epithelial lineage selection. Dev. Biol. 269, 252-263. (doi:10.1016/j.ydbio.2004.01.043)
77. Apte MV et al. 2004 Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas 29, 179-187. (doi:10.1097/00006676-200410000-00002)
78. Aoki H et al. 2006 Existence of autocrine loop between interleukin-6 and transforming growth factorbeta1 in activated rat pancreatic stellate cells. J. Cell. Biochem. 99, 221-228. (doi:10.1002/jcb.20906)
79. Bachem MG et al. 2005 Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. Gastroenterology 128, 907-921. (doi:10.1053/j.gastro.2004.12.036)
80. Grzesiak JJ, Ho JC, Moossa AR, Bouvet M. 2007 The integrin-extracellular matrix axis in pancreatic cancer. Pancreas 35, 293-301. (doi:10.1097/mpa.0b013e31811f4526)
81. Riopel MM, Li J, Liu S, Leask A, Wang R. 2013 β1 integrin-extracellular matrix interactions are essential for maintaining exocrine pancreas architecture and function. Lab. Invest. 93, 31-40. (doi:10.1038/labinvest.2012)
82. 1 integrins in a novel three-dimensional in vitro model of pancreatic cancer. Pancreas 34, 220-228. (doi:10.1097/01.mpa.0000250129.64650.f6)
83. 1 integrin mediates the malignant phenotype on type I collagen in pancreatic cancer cell lines. Br. J. Cancer 94, 1311-1319. (doi:10.1038/sj.bjc.6603088)
84. 5 promotes carcinoma cell invasion and metastasis. Cancer Res. 69, 1383-1391. (doi:10.1158/0008-5472.CAN-08-3612)
85. 1 integrin, and the cytoskeleton regulate pancreatic carcinoma cell IL8 secretion. Br. J. Cancer 91, 1327-1334. (doi:10.1038/sj.bjc. 6602132)
86. Paron I, Berchtold S, Vörös J, Shamarla M, Erkan M, Höfler H, Esposito I. 2011 Tenascin-C enhances pancreatic cancer cell growth and motility and affects cell adhesion through activation of the integrin pathway. PLoS ONE 6, e21684. (doi:10.1371/journal.pone.0021684)
87. Yee NS, Zhou W, Lee M. 2010 Transient receptor potential channel TRPM8 is over-expressed and required for cellular proliferation in pancreatic adenocarcinoma. Cancer Lett. 297, 49-55. (doi:10.1016/j.canlet.2010.04.023)
88. Rybarczyk P et al. 2012 Transient receptor potential melastatin-related 7 channel is overexpressed in human pancreatic ductal adenocarcinomas and regulates human pancreatic cancer cell migration. Int. J. Cancer 131, E851-E861. (doi:10.1002/ijc. 27487)
89. Yee NS, Zhou W, Liang IC. 2011 Transient receptor potential ion channel Trpm7 regulates exocrine pancreatic epithelial proliferation by Mg2+sensitive Socs3a signaling in development and cancer. Dis. Model. Mech. 4, 240-254. (doi:10.1242/dmm.004564)
90. 2+-mediated motility of human pancreatic duct cells. Am. J. Physiol. Cell Physiol. 299, C1493-C1503. (doi:10.1152/ajpcell. 00242.2010)
91. Arcangeli A et al. 2013 Prognostic significance and functional relevance of hERG1 potassium channel expression in pancreatic ductal adenocarcinoma. 47th Pancreas Club Meeting-17-18 May. P016.
92. + exchanger 1 by neurotensin signaling in pancreatic cancer cell lines. Biochem. Biophys. Res. Commun. 393, 414-419. (doi:10.1016/j.bbrc.2010. 02.009)
93. Provost JJ, Wallert MA. 2013 Inside out: targeting NHE1 as an intracellular and extracellular regulator of cancer progression. Chem. Biol. Drug Des. 81, 85-101. (doi:10.1111/cbdd.12035)
94. Miyamoto H, Murakami T, Tsuchida K, Sugino H, Miyake H, Tashiro S. 2004 Tumor-stroma interaction of human pancreatic cancer: acquired resistance to anticancer drugs and proliferation regulation is dependent on extracellular matrix proteins. Pancreas 28, 38-44. (doi:10.1097/00006676-200401000-00006)
95. Mantoni TS, Lunardi S, Al-Assar O, Masamune A, Brunner TB. 2011 Pancreatic stellate cells radioprotect pancreatic cancer cells through β1-integrin signaling. Cancer Res. 71, 3453-3458. (doi:10.1158/0008-5472.CAN-10-1633)