A mechanically-induced colon cancer cell population shows increased metastatic potential

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Tang, Xin ^a   Kuhlenschmidt, Theresa B ^b   Li, Qian ^b   Ali, Shahjahan ^c   Lezmi, Stephane ^b   Chen, Hong ^b   Pires Alves, Melissa ^b   Laegreid, William W ^b   Saif, Taher A ^a   Kuhlenschmidt, Mark S ^b  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Cancer biomarkers; In vitro cancer microenvironment; Invasiveness; Mechanotransduction; Metastasis; Polyacrylamide hydrogel

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 3A1; BONE MORPHOGENETIC PROTEIN 4; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; HLA E ANTIGEN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; AKR1B10 PROTEIN, HUMAN; ALDEHYDE REDUCTASE; ALDH3A1 PROTEIN, HUMAN; CLAUDIN; CLDN2 PROTEIN, HUMAN; HYDROGEL; TENSINS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATOMIC FORCE MICROSCOPY; CANCER CELL CULTURE; CELL MIGRATION; CLDN2 GENE; COLON CANCER; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MARKER GENE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; TNS4 GENE; TUMOR INVASION; ANIMAL; CANCER TRANSPLANTATION; CELL MOTION; CELL PROLIFERATION; CELL SHAPE; COLON; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; HYDROGEL; INTRALESIONAL DRUG ADMINISTRATION; LIVER TUMOR; MECHANOTRANSDUCTION; METABOLISM; NUDE MOUSE; PATHOLOGY; SECONDARY; SPLEEN; SPLEEN TUMOR; TUMOR CELL LINE;

ANIMALIA; MUS MUSCULUS;

ALDEHYDE DEHYDROGENASE; ALDEHYDE REDUCTASE; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CLAUDINS; COLON; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROGELS; INJECTIONS, INTRALESIONAL; LIVER NEOPLASMS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, NUDE; MICROFILAMENT PROTEINS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; SPLEEN; SPLENIC NEOPLASMS;

EID: 84903304046     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-131     Document Type: Article

References (79)

1. Weinberg RA. The Biology of Cancer 2007, New York: Garland Science.
2. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
3. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
4. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer 2001, 1:46-54.
5. Vogelstein B, Kinzler KW. Cancer genes and the pathways they control. Nat Med 2004, 10:789-799.
6. Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev 2002, 2:563-572.
7. Brábek J, Mierke CT, Rösel D, Veselý P, Fabry B. The role of the tissue microenvironment in the regulation of cancer cell motility and invasion. Cell Commun Signal 2010, 8:1-8.
8. Huang S, Ingber DE. Cell tension, matrix mechanics, and cancer development. Cancer Cell 2005, 8:175-176.
9. Mareel M, Oliveira MJ, Madani I. Cancer invasion and metastasis: interacting ecosystems. Virchows Arch 2009, 454:599-622.
10. Rosenthal KL, Tompkins WAF, Frank GL, McCulloch P, Rawls WE. Variants of a human colon adenocarcinoma cell line which differ in morphology and carcinoembryonic antigen production. Cancer Res 1977, 37:4024-4030.
11. Tompkins WA, Watrach AM, Schmale JD, Schultz RM, Harris JA. Cultural and antigenic properties of newly established cell strains derived from adenocarcinomas of the human colon and rectum. J Natl Cancer Inst 1974, 52:1101-1110.
12. Vermeulen SJ, Bruyneel EA, Bracke ME, Bruyne GKD, Vennekens KM, Vleminckx KL, Berx GJ, Roy FM, Mareel MM. Transition from the noninvasive to the invasive phenotype and loss of a-Catenin in human colon cancer cells. Cancer Res 1995, 55:4722-4728.
13. Vermeulen SJ, Chen TR, Speleman F, Nollet F, Roy FMV, Mareel MM. Did the four human cancer cell lines DLD-1, HCT-15, HCT-8, and HRT-18 originate from One and the same patient?. Cancer Genet Cytogenet 1998, 107:76-79.
14. Vermeulen SJ, Nollet F, Teugels E, Vennekens KM, Malfait F, Philippe T, Speleman F, Bracke ME, Roy FM, Mareel MM. The Alpha-E-catenin gene (CTNNA1) acts as an invasion-suppressor gene in human colon cancer cells. Oncogene 1999, 18:905-915.
15. Baker EL, Bonnecaze RT, Zaman MH. Extracellular matrix stiffness and architecture govern intracellular rheology in cancer. Biophys J 2009, 97:1013-1021.
16. Butcher DT, Alliston T, Weaver VM. A tense situation: forcing tumour progression. Nat Rev Cancer 2009, 9:108-122.
17. Kumar S, Weaver VM. Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 2009, 28:113-127.
18. Pathak A, Kumar S. Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integr Biol 2011, 3:267-278.
19. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, Damsky C, Bissell MJ. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 1997, 137:231-245.
20. Wirtz D, Konstantopoulos K, Searson PC. The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat Rev Cancer 2011, 11:512-522.
21. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SFT, Csiszar K, Giaccia A, Weninger W, Yamauchi M, Gasser DL, Weaver VM. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
22. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
23. Liu J, Tan Y, Zhang H, Zhang Y, Xu P, Chen J, Poh Y-C, Tang K, Wang N, Huang B. Soft fibrin gels promote selection and growth of tumorigenic cells. Nat Mater 2012, 11:734-741.
24. Califano JP, Reinhart-King CA. Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell Mol Bioeng 2010, 3:68-75.
25. Fu J, Wang Y-K, Yang MT, Desai RA, Yu X, Liu Z, Chen CS. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 2010, 7:733-736.
26. Tang X, Kuhlenschmidt TB, Zhou J, Bell P, Wang F, Kuhlenschmidt MS, Saif TA. Mechanical force affects expression of an in vitro metastasis-like phenotype in HCT-8 cells. Biophys J 2010, 99:2460-2469.
27. Tang X, Wen Q, Kuhlenschmidt TB, Kuhlenschmidt MS, Janmey PA, Saif TA. Attenuation of cell mechanosensitivity in colon cancer cells during in vitro metastasis. Plos ONE 2012, 7:e50443.
28. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, Scott EW, Huang EH. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 2009, 69:8208-8215.
29. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS, Boman BM. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009, 69:3382-3389.
30. Townsend AJ, Leone-Kabler S, Haynes RL, Wu Y, Szwed L, Bunting KD. Selective protection by stably transfected human ALDH3A1 (but not human ALDH1A1) against toxicity of aliphatic aldehydes in V79 cells. Chem Biol Interact 2001, 130:261-273.
31. Albasri A, Seth R, Jackson D, Benhasouna A, Crook S, Nateri AS, Chapman R, Ilyas M. C-terminal Tensin-like (CTEN) is an oncogene which alters cell motility possibly through repression of E-cadherin in colorectal cancer. J Pathol 2009, 218:57-65.
32. Dhawan P, Ahmad R, Chaturvedi R, Smith J, Midha R, Mittal M, Krishnan M, Chen X, Eschrich S, Yeatman T, Harris RC, Washington MK, Wilson KT, Beauchamp RD, Singh AB. Claudin-2 expression increases tumorigenicity of colon cancer cells: role of epidermal growth factor receptor activation. Oncogene 2011, 30:3234-3247.
33. Katz M, Amit I, Citri A, Shay T, Carvalho S, Lavi S, Milanezi F, Lyass L, Amariglio N, Jacob-Hirsch J, Ben-Chetrit N, Tarcic G, Lindzen M, Avraham R, Liao YC, Trusk P, Lyass A, Rechavi G, Spector NL, Lo SH, Schmitt F, Bacus SS, Yarden Y. A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration. Nat Cell Biol 2007, 9:961-969.
34. Liao Y-C, Chen N-T, Shih Y-P, Dong Y, Lo SH. Up-regulation of C-terminal Tensin-like molecule promotes the tumorigenicity of colon cancer through β-catenin. Cancer Res 2009, 69:4563.
35. Mooney SM, Rajagopalan K, Williams BH, Zeng Y, Christudass CS, Li Y, Yin B, Kulkarni P, Getzenberg RH. Creatine kinase brain overexpression protects colorectal cells from various metabolic and non-metabolic stresses. J Cell Biochem 2011, 112:1066-1075.
36. Cavallaro U, Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 2004, 4:118-132.
37. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
38. Matsunaga T, Wada Y, Endo S, Soda M, El-Kabbani O, Hara A. Aldo-Keto reductase 1B10 and its role in proliferation capacity of drug-resistant cancers. Front Pharmacol 2012, 3:1-11.
39. Moreb JS. Aldehyde dehydrogenase as a marker for stem cells. Curr Stem Cell Res Ther 2008, 3:237-246.
40. Yan R, Zu X, Ma J, Liu Z, Adeyanju M, Cao D. Aldo-keto reductase family 1 B10 gene silencing results in growth inhibition of colorectal cancer cells: Implication for cancer intervention. Int J Cancer 2007, 121:2301-2306.
41. Black W, Chen Y, Matsumoto A, Thompson DC, Lassen N, Pappa A, Vasiliou V. Molecular mechanisms of ALDH3A1-mediated cellular protection against 4-hydroxy-2-nonenal. Free Radic Biol Med 2012, 52:1937-1944.
42. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer C, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567.
43. Ma I, Allan AL. The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev Rep 2011, 7:292-306.
44. Fruehauf JP, L Meyskens F. Reactive oxygen species: a breath of life or death?. Clin Cancer Res 2007, 13:789-794.
45. Konorev EA, Zhang H, Joseph J, Kennedy MC, Kalyanaraman B. Bicarbonate exacerbates oxidative injury induced by antitumor antibiotic doxorubicin in cardiomyocytes. Am J Physiol Heart Circ Physiol 2000, 279:2424-2430.
46. Manda G, Nechifor MT, Neagu T-M. Reactive oxygen species, cancer and anti-cancer therapies. Curr Chem Biol 2009, 3:342-366.
47. Maurer BJ, Metelitsa LS, Seeger RC, Cabot MC, Reynolds CP. Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-Hydroxyphenyl)-retinamide in Neuroblastoma cell lines. J Nat Cancer Inst 1999, 91:1138-1146.
48. Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 2006, 5:1-8.
49. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
50. Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer 2006, 6:449-458.
51. Kim Y-N, Koo KH, Sung JY, Yun U-J, Kim H. Anoikis resistance: an essential prerequisite for tumor metastasis. Int J Cell Biol 2012, 2011:1-11.
52. Zhan M, Zhao H, Han ZC. Signalling mechanisms of anoikis. Histol Histopathol 2004, 19:973-983.
53. Simpson CD, Anyiwe K, Schimmer AD. Anoikis resistance and tumor metastasis. Cancer Lett 2008, 272:177-185.
54. Kantak SS, Kramer RH. E-cadherin regulates anchorage-independent growth and survival in oral squamous cell carcinoma cells. J Biol Chem 1998, 273:16953-16961.
55. Butler JP, Fredberg JJ, Ingber DE, Wang N. Method and system for measurement of mechanical properties of molecules and cells. US Patent Number US5486457, 2 March 1995.
56. Cross SE, Jin Y-S, Rao J, Gimzewski JK. Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2007, 2:780-783.
57. Guck J, Schinkinger S, Lincoln B, Wottawah F, Ebert S, Romeyke M, Len D, Erickson HM, Ananthakrishnan R, Mitchell D, Kas J, Ulvick S, Bilby C. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J 2005, 88:3689-3698.
58. Plodinec M, Loparic M, Monnier CA, Obermann EC, Zanetti-Dallenbach R, Oertle P, Hyotyla JT, Aebi U, Bentires-Alj M, Lim RYH, Schoenenberger C-A. The nanomechanical signature of breast cancer. Nat Nanotechnol 2012, 7:757-765.
59. Suresh S, Spatz J, Mills JP, Micoulet A, Dao M, Lim CT, Beil M, Seufferlein T. Connections between single-cell biomechanics and human disease states: gastrointestinal cancer and malaria. Acta Biomater 2005, 1:15-30.
60. Deng S, Yang X, Lassus H, Liang S, Kaur S, Ye Q, Li C, Wang L-P, Roby KF, Orsulic S, Connolly DC, Zhang Y, Montone K, Butzow R, Coukos G, Zhang L. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS ONE 2010, 5:1-11.
61. Marcato P, Dean CA, Pan D, Araslanova R, Gillis M, Joshi M, Helyer L, Pan L, Leidal A, Gujar S, Giacomantonio CA, Lee PW. Aldehyde dehydrogenase activity of breast cancer stem cells is primarily due to isoform ALDH1A3 and its expression is predictive of metastasis. Stem Cell 2011, 29:32-45.
62. Sl'adek NE. Human aldehyde dehydrogenases: potential pathological, pharmacological, and toxicological impact. J Biochem Mol Toxicol 2003, 17:7-23.
63. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, Gao B, Schuster K, Shao C, Larsen JE, Sullivan LA, Honorio S, Xie Y, Scaglioni PP, DiMaio JM, Gazdar AF, Shay JW, Wistuba II, Minna JD. Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 2010, 70:9937-9948.
64. Zhang Q, Taguchi A, Schliekelman M, Wong C-H, Chin A, Kuick RE, Misek D, Hanash S. Comprehensive proteomic profiling of aldehyde dehydrogenases in lung adenocarcinoma cell lines. Int J Proteomics 2011, 2011:1-8.
65. Muzio G, Maggiora M, Paiuzzi E, Oraldi M, Canut RA. Aldehyde dehydrogenases and cell proliferation. Free Radic Biol Med 2012, 52:735-746.
66. Bertucci F, Salas S, Eysteries S, Nasser V, Finetti P, Ginestier C, Charafe-Jauffret E, Loriod B, Bachelart L, Montfort J, Victorero G, Viret F, Ollendorff V, Fert V, Giovaninni M, Delpero JR, Nguyen C, Viens P, Monges G, Birnbaum D, Houlgatte R. Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters. Oncogene 2004, 23:1377-1391.
67. Al-Ghamdi S, Albasri A, Cachat J, Ibrahem S, Muhammad BA, Jackson D, Nateri AS, Kindle KB, Ilyas M. Cten is targeted by Kras signalling to regulate cell motility in the colon and pancreas. PloS ONE 2011, 6:1-8.
68. Hu G, Chong RA, Yang Q, Wei Y, Blanco MA, Li F, Reiss M, Au JL-S, Haffty BG, Kang Y. MTDH activation by 8q22 genomic gain promotes chemoresistance and metastasis of poor-prognosis breast cancer. Cancer Cell 2009, 15:9-20.
69. Berger MJ, Minnerath SR, Adams SD, Tigges BM, Sprague SL, McKenna DH. Gene expression changes with differentiation of cord blood stem cells to respiratory epithelial cells: a preliminary observation. Stem Cell Res Ther 2011, 2:1-8.
70. Khanna M, Chen C-H, Kimble-Hill A, Parajuli B, Perez-Miller S, Baskaran S, Kim J, Dria K, Vasiliou V, Mochly-Rosen D, Hurley TD. Discovery of a novel class of covalent inhibitor for aldehyde dehydrogenases. J Biol Chem 2011, 286:43486-43494.
71. Rekha GK, Sreerama L, Sladek NE. Intrinsic cellular resistance to oxazaphosphorines exhibited by a human colon carcinoma cell line expressing relatively large amounts of a class-3 aldehyde dehydrogenase. Biochem Pharmacol 1994, 48:1943-1952.
72. Tang X, Cappa T, Kuhlenschmidt T, Kuhlenschmidt M, Saif T. Specific and non-specific adhesion in cancer cells with various metastatic potentials. Mechanobiology of Cell-Cell and Cell-Matrix Interactionss 2011, 105-122. New York: Springer US, Johnson AW, Harley B.
73. Tang X, Bajaj P, Bashir R, Saif TA. How far cardiac cells can see each other mechanically. Soft Matter 2011, 7:6151-6158.
74. Tang X, Ali MY, Saif MTA. A novel technique for micro-patterning proteins and cells on polyacrylamide gels. Soft Matter 2012, 8:7197-7206.
75. Bajaj P, Tang X, Saif TA, Bashir R. Stiffness of the substrate influences the phenotype of embryonic chicken cardiac myocytes. J Biomed Mater Res A 2010, 95:1261-1269.
76. Cha C, Jeong JH, Tang X, Zill AT, Prakash YS, Zimmerman SC, Saif TA, Kong H. Top-down synthesis of versatile polyaspartamide linkers for single-step protein conjugation to materials. Bioconjug Chem 2011, 22:2377-2382.
77. Dong R, Jensen TW, Engberg K, Nuzzo RG, Leckband DE. Variably elastic hydrogel patterned via capillary action in microchannels. Langmuir 2007, 23:1483-1488.
78. Brandt R, Keston AS. Synthesis of diacetyldichlorofluorescin: a stable reagent for fluorometric analysis. Anal Biochem 1965, 11:6-9.
79. Jakubowski W, Bartosz G. 2,7-dichlorofluorescin oxidation and reactive oxygen species: what does it measure?. Cell Biol Int 2000, 24:757-760.