Changes in cellular mechanical properties during onset or progression of colorectal cancer

World Journal of Gastroenterology

Volumn 22, Issue 32, 2016, Pages 7203-7214

  Ciasca, Gabriele ^a   Papi, Massimiliano ^a   Minelli, Eleonora ^a   Palmieri, Valentina ^a   De Spirito, Marco ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

Atomic force microscopy; Biomechanics; Colorectal cancer; Mechanical signalling; Pressure; Wnt

Indexed keywords

CANCER CELL; CANCER GROWTH; CELL DIFFERENTIATION; CELL PROLIFERATION; COLORECTAL CANCER; DISEASE ASSOCIATION; EARLY CANCER; EXTRACELLULAR MATRIX; EXTRAVASATION; HUMAN; MECHANOTRANSDUCTION; METASTATIC COLON CANCER; NONHUMAN; RELAXATION TRAINING; REVIEW; SHEAR STRESS; TUMOR MICROENVIRONMENT; WNT SIGNALING PATHWAY; ANIMAL; BIOMECHANICS; CELL TRANSFORMATION; COLORECTAL NEOPLASMS; DISEASE COURSE; GENETICS; MOUSE; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR SUPPRESSOR GENE;

ANIMALS; BIOMECHANICAL PHENOMENA; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; GENES, APC; HUMANS; MICE; MUTATION; TUMOR MICROENVIRONMENT; WNT SIGNALING PATHWAY;

EID: 84983480687     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v22.i32.7203     Document Type: Review

References (95)

1. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut 2016; Epub ahead of print [PMID: 26818619 DOI: 10.1136/gutjnl-2015-310912]
2. Gout S, Huot J. Role of cancer microenvironment in metastasis: focus on colon cancer. Cancer Microenviron 2008; 1: 69-83 [PMID: 19308686 DOI: 10.1007/s12307-008-0007-2]
3. Boland CR, Goel A. Microsatellite instability in colorectal cancer. Gastroenterology 2010; 138: 2073-2087.e3 [PMID: 20420947 DOI: 10.1053/j.gastro.2009.12.064]
4. Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6: 479-507 [PMID: 21090969 DOI: 10.1146/annurevpathol-011110-130235]
5. Fernández-Sánchez ME, Barbier S, Whitehead J, Béalle G, Michel A, Latorre-Ossa H, Rey C, Fouassier L, Claperon A, Brullé L, Girard E, Servant N, Rio-Frio T, Marie H, Lesieur S, Housset C, Gennisson JL, Tanter M, Ménager C, Fre S, Robine S, Farge E. Mechanical induction of the tumorigenic β-catenin pathway by tumour growth pressure. Nature 2015; 523: 92-95 [PMID: 25970250 DOI: 10.1038/nature14329]
6. Whitehead J, Vignjevic D, Fütterer C, Beaurepaire E, Robine S, Farge E. Mechanical factors activate beta-catenin-dependent oncogene expression in APC mouse colon. HFSP J 2008; 2: 286-294 [PMID: 19404440 DOI: 10.2976/1.2955566]
7. Smallwood RH, Holcombe WM, Walker DC. Development and validation of computational models of cellular interaction. J Mol Histol 2004; 35: 659-665 [PMID: 15614621 DOI: 10.1007/s10735-004-2660-1]
8. Walker DC, Southgate J, Hill G, Holcombe M, Hose DR, Wood SM, Mac Neil S, Smallwood RH. The epitheliome: agent-based modelling of the social behaviour of cells. Biosystems 2004; 76: 89-100 [PMID: 15351133 DOI: 10.1016/j.biosystems.2004.05.025]
9. Galle J, Loeffler M, Drasdo D. Modeling the effect of deregulated proliferation and apoptosis on the growth dynamics of epithelial cell populations in vitro. Biophys J 2005; 88: 62-75 [PMID: 15475585 DOI: 10.1529/biophysj.104.041459]
10. Meineke FA, Potten CS, Loeffler M. Cell migration and organization in the intestinal crypt using a lattice-free model. Cell Prolif 2001; 34: 253-266 [PMID: 11529883 DOI: 10.1046/j.0960-7722.2001.00216.x]
11. Morel D, Marcelpoil R, Brugal G. A proliferation control network model: the simulation of two-dimensional epithelial homeostasis. Acta Biotheor 2001; 49: 219-234 [PMID: 11804235 DOI: 10.1023/A:1014201805222]
12. Drasdo D, Loeffler M. Individual-based models to growth and folding in one-layered tissues: intestinal crypts and early development. Nonlinear Analysis: Theory, Methods & Applications 2001; 47: 245-256 [DOI: 10.1016/S0362-546X(01)00173-0]
13. van Leeuwen IM, Byrne HM, Jensen OE, King JR. Crypt dynamics and colorectal cancer: advances in mathematical modelling. Cell Prolif 2006; 39: 157-181 [PMID: 16671995 DOI: 10.1111/j.1365-2184.2006.00378.x]
14. Loeffler M, Stein R, Wichmann HE, Potten CS, Kaur P, Chwalinski S. Intestinal cell proliferation. I. A comprehensive model of steadystate proliferation in the crypt. Cell Tissue Kinet 1986; 19: 627-645 [PMID: 3802185 DOI: 10.1111/j.1365-2184.1986.tb00763.x]
15. Loeffler M, Potten CS, Paulus U, Glatzer J, Chwalinski S. Intestinal crypt proliferation. II. Computer modelling of mitotic index data provides further evidence for lateral and vertical cell migration in the absence of mitotic activity. Cell Tissue Kinet 1988; 21: 247-258 [PMID: 3233644 DOI: 10.1111/j.1365-2184.1988. tb00784.x]
16. Paulus U, Loeffler M, Zeidler J, Owen G, Potten CS. The differentiation and lineage development of goblet cells in the murine small intestinal crypt: experimental and modelling studies. J Cell Sci 1993; 106 (Pt 2): 473-483 [PMID: 8282755]
17. Gerike TG, Paulus U, Potten CS, Loeffler M. A dynamic model of proliferation and differentiation in the intestinal crypt based on a hypothetical intraepithelial growth factor. Cell Prolif 1998; 31: 93-110 [PMID: 9745618 DOI: 10.1046/j.1365-2184.1998.00113.x]
18. Edwards CM, Chapman SJ. Biomechanical modelling of colorectal crypt budding and fission. Bull Math Biol 2007; 69: 1927-1942 [PMID: 17443390 DOI: 10.1007/s11538-007-9199-8]
19. Boman BM, Fields JZ, Bonham-Carter O, Runquist OA. Computer modeling implicates stem cell overproduction in colon cancer initiation. Cancer Res 2001; 61: 8408-8411 [PMID: 11731419]
20. Palmieri V, Lucchetti D, Maiorana A, Papi M, Maulucci G, Calapà F, Ciasca G, Giordano R, Sgambato A, De Spirito M. Mechanical and structural comparison between primary tumor and lymph node metastasis cells in colorectal cancer. Soft Matter 2015; 11: 5719-5726 [PMID: 26083581 DOI: 10.1039/c5sm01089f]
21. Palmieri V, Lucchetti D, Maiorana A, Papi M, Maulucci G, Ciasca G, Svelto M, De Spirito M, Sgambato A. Biomechanical investigation of colorectal cancer cells. Appl Phys Lett 2014; 105: 123701
22. Liu J, Tan Y, Zhang H, Zhang Y, Xu P, Chen J, Poh YC, Tang K, Wang N, Huang B. Soft fibrin gels promote selection and growth of tumorigenic cells. Nat Mater 2012; 11: 734-741 [PMID: 22751180 DOI: 10.1038/nmat3361]
23. Tang X, Kuhlenschmidt TB, Li Q, Ali S, Lezmi S, Chen H, Pires-Alves M, Laegreid WW, Saif TA, Kuhlenschmidt MS. A mechanically-induced colon cancer cell population shows increased metastatic potential. Mol Cancer 2014; 13: 131 [PMID: 24884630 DOI: 10.1186/1476-4598-13-131]
24. 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 [PMID: 20959086 DOI: 10.1016/j.bpj.2010.08.034]
25. 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 [PMID: 23226284 DOI: 10.1371/journal.pone.0050443]
26. Pachenari M, Seyedpour SM, Janmaleki M, Babazadeh Shayan S, Taranejoo S, Hosseinkhani H. Mechanical properties of cancer cytoskeleton depend on actin filaments to microtubules content: investigating different grades of colon cancer cell lines. J Biomech 2014; 47: 373-379 [PMID: 24315289 DOI: 10.1016/j.jbiomech.2013.11.020]
27. Avvisato CL, Yang X, Shah S, Hoxter B, Li W, Gaynor R, Pestell R, Tozeren A, Byers SW. Mechanical force modulates global gene expression and beta-catenin signaling in colon cancer cells. J Cell Sci 2007; 120: 2672-2682 [PMID: 17635998 DOI: 10.1242/jcs.03476]
28. Peddareddigari VG, Wang D, Dubois RN. The tumor microenvironment in colorectal carcinogenesis. Cancer Microenviron 2010; 3: 149-166 [PMID: 21209781 DOI: 10.1007/s12307-010-0038-3]
29. Suresh S. Biomechanics and biophysics of cancer cells. Acta Biomater 2007; 3: 413-438 [PMID: 17540628 DOI: 10.1016/j.actbio.2007. 04.002]
30. Lekka M. Atomic force microscopy: A tip for diagnosing cancer. Nat Nanotechnol 2012; 7: 691-692 [PMID: 23132222 DOI: 10.1038/nnano.2012.196]
31. Lekka M, Gil D, Pogoda K, Dulińska-Litewka J, Jach R, Gostek J, Klymenko O, Prauzner-Bechcicki S, Stachura Z, Wiltowska-Zuber J, Okoń K, Laidler P. Cancer cell detection in tissue sections using AFM. Arch Biochem Biophys 2012; 518: 151-156 [PMID: 22209753 DOI: 10.1016/j.abb.2011.12.013]
32. Lekka M, Laidler P. Applicability of AFM in cancer detection. Nat Nanotechnol 2009; 4: 72; author reply 72-73 [PMID: 19197298 DOI: 10.1038/nnano.2009.004]
33. Lekka M, Pogoda K, Gostek J, Klymenko O, Prauzner-Bechcicki S, Wiltowska-Zuber J, Jaczewska J, Lekki J, Stachura Z. Cancer cell recognition-mechanical phenotype. Micron 2012; 43: 1259-1266 [PMID: 22436422 DOI: 10.1016/j.micron.2012.01.019]
34. Goetz JG, Minguet S, Navarro-Lérida I, Lazcano JJ, Samaniego R, Calvo E, Tello M, Osteso-Ibáñez T, Pellinen T, Echarri A, Cerezo A, Klein-Szanto AJ, Garcia R, Keely PJ, Sánchez-Mateos P, Cukierman E, Del Pozo MA. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011; 146: 148-163 [PMID: 21729786 DOI: 10.1016/j.cell.2011.05.040]
35. Butcher DT, Alliston T, Weaver VM. A tense situation: forcing tumour progression. Nat Rev Cancer 2009; 9: 108-122 [PMID: 19165226 DOI: 10.1038/nrc2544]
36. Cross SE, Jin YS, Rao J, Gimzewski JK. Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2007; 2: 780-783 [PMID: 18654431 DOI: 10.1038/nnano.2007.388]
37. DuFort CC, Paszek MJ, Weaver VM. Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 2011; 12: 308-319 [PMID: 21508987 DOI: 10.1038/nrm3112]
38. Hayashi K, Iwata M. Stiffness of cancer cells measured with an AFM indentation method. J Mech Behav Biomed Mater 2015; 49: 105-111 [PMID: 26004036 DOI: 10.1016/j.jmbbm.2015.04.030]
39. Katira P, Bonnecaze RT, Zaman MH. Modeling the mechanics of cancer: effect of changes in cellular and extra-cellular mechanical properties. Front Oncol 2013; 3: 145 [PMID: 23781492 DOI: 10.3389/fonc.2013.00145]
40. 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 [PMID: 21701513]
41. Friedl P, Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011; 147: 992-1009 [PMID: 22118458 DOI: 10.1016/j.cell.2011.11.016]
42. Tian M, Li Y, Liu W, Jin L, Jiang X, Wang X, Ding Z, Peng Y, Zhou J, Fan J, Cao Y, Wang W, Shi Y. The nanomechanical signature of liver cancer tissues and its molecular origin. Nanoscale 2015; 7: 12998-13010 [PMID: 26168746 DOI: 10.1039/c5nr02192h]
43. Hirokawa M, Miura S, Kishikawa H, Yoshida H, Nakamizo H, Higuchi H, Nakatsumi RC, Suzuki H, Saito H, Ishii H. Loading of mechanical pressure activates mitogen-activated protein kinase and early immediate gene in intestinal epithelial cells. Dig Dis Sci 2001; 46: 1993-2003 [PMID: 11575455]
44. Hirokawa M, Miura S, Shigematsu T, Yoshida H, Hokari R, Higuchi H, Kurose I, Kimura H, Saito H, Nakaki T, Ishii H. Pressure stimulates proliferation and DNA synthesis in rat intestinal epithelial cells. Life Sci 1997; 61: 667-672 [PMID: 9252241 DOI: 10.1016/S0024-3205(97)00531-6]
45. Ali MY, Saif MT. Substrate Stiffness Mediated Metastasis Like Phenotype of Colon Cancer Cells is Independent of Cell to Gel Adhesion. Cell Mol Bioeng 2014; 7: 532-543 [DOI: 10.1007/s12195-014-0345-8]
46. Vermeulen SJ, Bruyneel EA, Bracke ME, De Bruyne GK, Vennekens KM, Vleminckx KL, Berx GJ, van Roy FM, Mareel MM. Transition from the noninvasive to the invasive phenotype and loss of alpha-catenin in human colon cancer cells. Cancer Res 1995; 55: 4722-4728 [PMID: 7553655]
47. Vermeulen SJ, Chen TR, Speleman F, Nollet F, Van Roy FM, 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 [PMID: 9809040]
48. Vermeulen SJ, Nollet F, Teugels E, Vennekens KM, Malfait F, Philippé J, Speleman F, Bracke ME, van Roy FM, Mareel MM. The alphaE-catenin gene (CTNNA1) acts as an invasionsuppressor gene in human colon cancer cells. Oncogene 1999; 18: 905-915 [PMID: 10023666 DOI: 10.1038/sj.onc.1202348]
49. Hartono D, Liu Y, Tan PL, Then XY, Yung LY, Lim KM. Onchip measurements of cell compressibility via acoustic radiation. Lab Chip 2011; 11: 4072-4080 [PMID: 22020269 DOI: 10.1039/c1lc20687g]
50. Nagrath S, Sequist LV, Maheswaran S, Bell DW, Irimia D, Ulkus L, Smith MR, Kwak EL, Digumarthy S, Muzikansky A, Ryan P, Balis UJ, Tompkins RG, Haber DA, Toner M. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 2007; 450: 1235-1239 [PMID: 18097410 DOI: 10.1038/nature06385]
51. Giavazzi R, Foppolo M, Dossi R, Remuzzi A. Rolling and adhesion of human tumor cells on vascular endothelium under physiological flow conditions. J Clin Invest 1993; 92: 3038-3044 [PMID: 7504697 DOI: 10.1172/JCI116928]
52. Humphries A, Wright NA. Colonic crypt organization and tumorigenesis. Nat Rev Cancer 2008; 8: 415-424 [PMID: 18480839 DOI: 10.1038/nrc2392]
53. Crosnier C, Stamataki D, Lewis J. Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 2006; 7: 349-359 [PMID: 16619050 DOI: 10.1038/nrg1840]
54. Barker N, van de Wetering M, Clevers H. The intestinal stem cell. Genes Dev 2008; 22: 1856-1864 [PMID: 18628392 DOI: 10.1101/gad.1674008]
55. Ekins-Daukes N, Kawaguchi K, Zhang J. Strain-balanced criteria for multiple quantum well structures and its signature in X-ray rocking curves. Cryst Growth Des 2002; 2: 287-292 [DOI: 10.1021/cg025502y]
56. Ciasca G, De Seta M, Capellini G, Evangelisti F, Ortolani M, Virgilio M, Grosso G, Nucara A, Calvani P. Terahertz intersubband absorption and conduction band alignment in n-type Si/SiGe multiple quantum wells. Physic Rev B 2009; 79: 085302
57. Drasdo D. Buckling instabilities of one-layered growing tissues. Phys Rev Lett 2000; 84: 4244-4247 [PMID: 10990656 DOI: 10.1103/PhysRevLett.84.4244]
58. Nelson MR, Howard D, Jensen OE, King JR, Rose FR, Waters SL. Growth-induced buckling of an epithelial layer. Biomech Model Mechanobiol 2011; 10: 883-900 [PMID: 21191628 DOI: 10.1007/s10237-010-0280-0]
59. van Leeuwen IM, Edwards CM, Ilyas M, Byrne HM. Towards a multiscale model of colorectal cancer. World J Gastroenterol 2007; 13: 1399-1407 [PMID: 17457972 DOI: 10.3748/wjg.v13.i9.1399]
60. Basson MD. Paradigms for mechanical signal transduction in the intestinal epithelium. Category: molecular, cell, and developmental biology. Digestion 2003; 68: 217-225 [PMID: 14739529 DOI: 10.1159/000076385]
61. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006; 6: 392-401 [PMID: 16572188 DOI: 10.1038/nrc1877]
62. Dregelid E, Svendsen E. Endothelial cell injury in human saphenous veins after manipulation and tweezer grasping. J Cardiovasc Surg (Torino) 1988; 29: 464-469 [PMID: 3417749]
63. Basson MD, Yu CF, Herden-Kirchoff O, Ellermeier M, Sanders MA, Merrell RC, Sumpio BE. Effects of increased ambient pressure on colon cancer cell adhesion. J Cell Biochem 2000; 78: 47-61 [PMID: 10797565 DOI: 10.1002/(SICI)1097-4644(2000070 1)78:1<47::AID-JCB5>3.0.CO;2-M]
64. Basson MD, Modlin IM, Madri JA. Human enterocyte (Caco-2) migration is modulated in vitro by extracellular matrix composition and epidermal growth factor. J Clin Invest 1992; 90: 15-23 [PMID: 1634605 DOI: 10.1172/JCI115828]
65. Thamilselvan V, Basson MD. Pressure activates colon cancer cell adhesion by inside-out focal adhesion complex and actin cytoskeletal signaling. Gastroenterology 2004; 126: 8-18 [PMID: 14699482 DOI: 10.1053/j.gastro.2003.10.078]
66. Gutt CN, Kim ZG, Gessmann T, Lorenz M, Paolucci V. Hepatic tumor spread of colorectal cancer in a laparoscopic animal model. Surg Endosc 2000; 14: 448-451 [PMID: 10858469 DOI: 10.1007/s004640000159]
67. Groulx JF, Giroux V, Beauséjour M, Boudjadi S, Basora N, Carrier JC, Beaulieu JF. Integrin α6A splice variant regulates proliferation and the Wnt/β-catenin pathway in human colorectal cancer cells. Carcinogenesis 2014; 35: 1217-1227 [PMID: 24403311 DOI: 10.1093/carcin/bgu006]
68. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, 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 [PMID: 19931152 DOI: 10.1016/j.cell.2009.10.027]
69. 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 [PMID: 16169468 DOI: 10.1016/j.ccr.2005.08.010]
70. 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: 22 [PMID: 20822526 DOI: 10.1186/1478-811X-8-22]
71. Huang S, Ingber DE. Cell tension, matrix mechanics, and cancer development. Cancer Cell 2005; 8: 175-176 [PMID: 16169461 DOI: 10.1016/j.ccr.2005.08.009]
72. Rosenthal KL, Tompkins WA, 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 [PMID: 908038]
73. 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 [PMID: 21308735 DOI: 10.1002/jcb.23020]
74. 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 [PMID: 22406320 DOI: 10.1016/j.freer adbiomed.2012.02.050]
75. Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol 2003; 163: 1233-1243 [PMID: 14507633 DOI: 10.1016/S0002-9440(10)63483-9]
76. Mizukami Y, Kohgo Y, Chung DC. Hypoxia inducible factor-1 independent pathways in tumor angiogenesis. Clin Cancer Res 2007; 13: 5670-5674 [PMID: 17908955 DOI: 10.1158/1078-0432. CCR-07-0111]
77. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010; 141: 52-67 [PMID: 20371345 DOI: 10.1016/j.cell.2010.03.015]
78. Tsuji T, Sasaki Y, Tanaka M, Hanabata N, Hada R, Munakata A. Microvessel morphology and vascular endothelial growth factor expression in human colonic carcinoma with or without metastasis. Lab Invest 2002; 82: 555-562 [PMID: 12003996 DOI: 10.1038/labinvest.3780450]
79. Tien YW, Jeng YM, Hu RH, Chang KJ, Hsu SM, Lee PH. Intravasation-related metastatic factors in colorectal cancer. Tumour Biol 2004; 25: 48-55 [PMID: 15192312 DOI: 10.1159/000077723]
80. Mehlen P, Puisieux A. Metastasis: a question of life or death. Nat Rev Cancer 2006; 6: 449-458 [PMID: 16723991 DOI: 10.1038/nrc1886]
81. Chambers AF, Naumov GN, Varghese HJ, Nadkarni KV, MacDonald IC, Groom AC. Critical steps in hematogenous metastasis: an overview. Surg Oncol Clin N Am 2001; 10: 243-55, vii [PMID: 11382585]
82. Hochmuth RM. Micropipette aspiration of living cells. J Biomech 2000; 33: 15-22 [PMID: 10609514 DOI: 10.1016/S0021-9290(99)00175-X]
83. Tomaiuolo G. Biomechanical properties of red blood cells in health and disease towards microfluidics. Biomicrofluidics 2014; 8: 051501 [PMID: 25332724 DOI: 10.1063/1.4895755]
84. Sharma S, Gimzewski JK. Application of AFM to the Nanomechanics of Cancer. MRS Advances: 1-11 [DOI: 10.1557/adv.2016.255]
85. Ciasca G, Papi M, Di Claudio S, Chiarpotto M, Palmieri V, Maulucci G, Nocca G, Rossi C, De Spirito M. Mapping viscoelastic properties of healthy and pathological red blood cells at the nanoscale level. Nanoscale 2015; 7: 17030-17037 [PMID: 26415744 DOI: 10.1039/c5nr03145a]
86. De Spirito M, Brunelli R, Mei G, Bertani FR, Ciasca G, Greco G, Papi M, Arcovito G, Ursini F, Parasassi T. Low density lipoprotein aged in plasma forms clusters resembling subendothelial droplets: aggregation via surface sites. Biophys J 2006; 90: 4239-4247 [PMID: 16533854 DOI: 10.1529/biophysj.105.075788]
87. Di Gaspare L, Ciasca G, Pea M, Notargiacomo A. Ion and plasma based treatments for enhanced chemical speciation of metals in ferritin. Microelectron Eng 2014; 124: 86-89 [DOI: 10.1016/j.mee.2014.06.003]
88. Maiorana A, Bugli F, Papi M, Torelli R, Ciasca G, Maulucci G, Palmieri V, Cacaci M, Paroni Sterbini F, Posteraro B. Effect of alginate lyase on biofilm-grown Helicobacter pylori probed by atomic force microscopy. Int J Poly Sci 2015; 2015 [DOI: 10.1155/2015/989516]
89. Papi M, Lauriola M, Palmieri V, Ciasca G, Maulucci G, De Spirito M. Plasma protein corona reduces the haemolytic activity of graphene oxide nano and micro flakes. RSC Advances 2015; 5: 81638-81641 [DOI: 10.1039/C5RA15083C]
90. Lekka M. Discrimination Between Normal and Cancerous Cells Using AFM. Bionanoscience 2016; 6: 65-80 [PMID: 27014560 DOI: 10.1007/s12668-016-0191-3]
91. Boccaccio A, Papi M, De Spirito M, Lamberti L, Pappalettere C. Effect of the residual stress on soft sample nanoindentation. Appl Phys Lett 2013; 102: 133704 [DOI: 10.1063/1.4801428]
92. Frassanito M, Papi M, De Spirito M, Lamberti L, Boccaccio A, Arcovito G, Pappalettere C. Investigation of Zona Pellucida hardening with Atomic Force Microscopy and nonlinear optimization. 2011. Available from: URL: http://hdl.handle.net/10807/17321
93. Doriot PA, Dorsaz PA, Dorsaz L, De Benedetti E, Chatelain P, Delafontaine P. In-vivo measurements of wall shear stress in human coronary arteries. Coron Artery Dis 2000; 11: 495-502 [PMID: 10966136]
94. Yoon WH, Lee SK, Song KS, Kim JS, Kim TD, Li G, Yun EJ, Heo JY, Jung YJ, Park JI, Kweon GR, Koo SH, Park HD, Hwang BD, Lim K. The tumorigenic, invasive and metastatic potential of epithelial and round subpopulations of the SW480 human colon cancer cell line. Mol Med Rep 2008; 1: 763-768 [PMID: 21479483 DOI: 10.3892/mmr-00000026]
95. McDonald SA, Preston SL, Lovell MJ, Wright NA, Jankowski JA. Mechanisms of disease: from stem cells to colorectal cancer. Nat Clin Pract Gastroenterol Hepatol 2006; 3: 267-274 [PMID: 16673006 DOI: 10.1038/ncpgasthep0473]