Skip to main content

Advertisement

SpringerLink
Log in

Cohesive cancer invasion of the biophysical barrier of smooth muscle

  • Non-Thematic Review
  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Abstract

Smooth muscle is found around organs in the digestive, respiratory, and reproductive tracts. Cancers arising in the bladder, prostate, stomach, colon, and other sites progress from low-risk disease to high-risk, lethal metastatic disease characterized by tumor invasion into, within, and through the biophysical barrier of smooth muscle. We consider here the unique biophysical properties of smooth muscle and how cohesive clusters of tumor use mechanosensing cell–cell and cell–ECM (extracellular matrix) adhesion receptors to move through a structured muscle and withstand the biophysical forces to reach distant sites. Understanding integrated mechanosensing features within tumor cluster and smooth muscle and potential triggers within adjacent adipose tissue, such as the unique damage-associated molecular pattern protein (DAMP), eNAMPT (extracellular nicotinamide phosphoribosyltransferase), or visfatin, offers an opportunity to prevent the first steps of invasion and metastasis through the structured muscle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

N/A

References

  1. Society, A. C. (2020). Cancer Facts & Figures 2020. Atlanta, GA: American Cancer Society.

    Google Scholar 

  2. Beunk, L., Brown, K., Nagtegaal, I., Friedl, P., & Wolf, K. (2019). Cancer invasion into musculature: mechanics, molecules and implications. Seminars in Cell & Developmental Biology, 93, 36–45. https://doi.org/10.1016/j.semcdb.2018.07.014.

    Article  CAS  Google Scholar 

  3. Miller, V. M. (2009). Vascular biology In J. W. Hallett, J. L. Mills, J. J. Earnshaw, J. A. Reekers, & T. W. Rooke (Eds.), Comprehensive vascular and endovascular surgery (second edition) (pp. 12–20). Philadelphia: Mosby.

  4. Noone AM, H. N., Krapcho M, Miller D, Brest A, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds) (2018). SEER cancer statistics review, 1975–2015. https://seer.cancer.gov/archive/csr/1975_2015/#citation. Accessed Feb 23 2020.

  5. Kensler, K. H., & Rebbeck, T. R. (2020). Cancer progress and priorities: prostate cancer. Cancer Epidemiology, Biomarkers & Prevention, 29(2), 267–277. https://doi.org/10.1158/1055-9965.Epi-19-0412.

    Article  Google Scholar 

  6. Harryman, W. L., Hinton, J. P., Rubenstein, C. P., Singh, P., Nagle, R. B., Parker, S. J., et al. (2016). The cohesive metastasis phenotype in human prostate cancer. Biochimica et Biophysica Acta, 1866(2), 221–231. https://doi.org/10.1016/j.bbcan.2016.09.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Friedl, P., & Gilmour, D. (2009). Collective cell migration in morphogenesis, regeneration and cancer. Nature Reviews. Molecular Cell Biology, 10(7), 445–457. https://doi.org/10.1038/nrm2720.

    Article  CAS  PubMed  Google Scholar 

  8. Olson, A., Le, V., Aldahl, J., Yu, E. J., Hooker, E., He, Y., et al. (2019). The comprehensive role of E-cadherin in maintaining prostatic epithelial integrity during oncogenic transformation and tumor progression. PLoS Genetics, 15(10), e1008451. https://doi.org/10.1371/journal.pgen.1008451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lin, C.-Y., & Chuu, C.-P. (2016). Friend or foe: role of E-cadherin in prostate cancer metastasis. Translational Andrology and Urology, 5(6), 961–963. https://doi.org/10.21037/tau.2016.11.08.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Luo, K. J., Hu, Y., Wen, J., & Fu, J. H. (2011). CyclinD1, p53, E-cadherin, and VEGF discordant expression in paired regional metastatic lymph nodes of esophageal squamous cell carcinoma: a tissue array analysis. Journal of Surgical Oncology, 104(3), 236–243. https://doi.org/10.1002/jso.21921.

    Article  CAS  PubMed  Google Scholar 

  11. Bukholm, I. K., Nesland, J. M., & Børresen-Dale, A. L. (2000). Re-expression of E-cadherin, alpha-catenin and beta-catenin, but not of gamma-catenin, in metastatic tissue from breast cancer patients [see comments]. The Journal of Pathology, 190(1), 15–19. https://doi.org/10.1002/(sici)1096-9896(200001)190:1<15::Aid-path489>3.0.Co;2-l.

    Article  CAS  PubMed  Google Scholar 

  12. Jurčić, P., Radulović, P., Balja, M. P., Milošević, M., & Krušlin, B. (2019). E-cadherin and NEDD9 expression in primary colorectal cancer, metastatic lymph nodes and liver metastases. Oncology Letters, 17(3), 2881–2889. https://doi.org/10.3892/ol.2019.9917.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Nagle, R. B., & Cress, A. E. (2011). Metastasis update: human prostate carcinoma invasion via tubulogenesis. Prostate Cancer, 2011, 249290. https://doi.org/10.1155/2011/249290.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sroka, I. C., Anderson, T. A., McDaniel, K. M., Nagle, R. B., Gretzer, M. B., & Cress, A. E. (2010). The laminin binding integrin α6β1 in prostate cancer perineural invasion. Journal of Cellular Physiology, 224(2), 283–288. https://doi.org/10.1002/jcp.22149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Pouliot, N., & Kusuma, N. (2013). Laminin-511: a multi-functional adhesion protein regulating cell migration, tumor invasion and metastasis. Cell Adhesion & Migration, 7(1), 142–149. https://doi.org/10.4161/cam.22125.

    Article  Google Scholar 

  16. Pozzi, A., Yurchenco, P. D., & Iozzo, R. V. (2017). The nature and biology of basement membranes. Matrix Biology, 57-58, 1–11. https://doi.org/10.1016/j.matbio.2016.12.009.

    Article  CAS  PubMed  Google Scholar 

  17. Laurent, V., Toulet, A., Attane, C., Milhas, D., Dauvillier, S., Zaidi, F., et al. (2019). Periprostatic adipose tissue favors prostate cancer cell invasion in an obesity-dependent manner: role of oxidative stress. Molecular Cancer Research, 17(3), 821–835. https://doi.org/10.1158/1541-7786.Mcr-18-0748.

    Article  CAS  PubMed  Google Scholar 

  18. Nassar, Z. D., Aref, A. T., Miladinovic, D., Mah, C. Y., Raj, G. V., Hoy, A. J., et al. (2018). Peri-prostatic adipose tissue: the metabolic microenvironment of prostate cancer. BJU International, 121(Suppl 3), 9–21. https://doi.org/10.1111/bju.14173.

    Article  PubMed  Google Scholar 

  19. Gandaglia, G., Abdollah, F., Schiffmann, J., Trudeau, V., Shariat, S. F., Kim, S. P., et al. (2014). Distribution of metastatic sites in patients with prostate cancer: a population-based analysis. Prostate, 74(2), 210–216. https://doi.org/10.1002/pros.22742.

    Article  PubMed  Google Scholar 

  20. Surov, A., Hainz, M., Holzhausen, H. J., Arnold, D., Katzer, M., Schmidt, J., et al. (2010). Skeletal muscle metastases: primary tumours, prevalence, and radiological features. European Radiology, 20(3), 649–658. https://doi.org/10.1007/s00330-009-1577-1.

    Article  PubMed  Google Scholar 

  21. Coman, D. R., & de, L. R. (1951). The role of the vertebral venous system in the metastasis of cancer to the spinal column; experiments with tumor-cell suspensions in rats and rabbits. Cancer, 4(3), 610–618. https://doi.org/10.1002/1097-0142(195105)4:3<610::aid-cncr2820040312>3.0.co;2-q.

    Article  CAS  PubMed  Google Scholar 

  22. Nishijima, Y., Uchida, K., Koiso, K., & Nemoto, R. (1992). Clinical significance of the vertebral vein in prostate cancer metastasis. Advances in Experimental Medicine and Biology, 324, 93–100. https://doi.org/10.1007/978-1-4615-3398-6_9.

    Article  CAS  PubMed  Google Scholar 

  23. Batson, O. V. (1940). The function of the vertebral veins and their role in the spread of metastases. Annals of Surgery, 112(1), 138–149. https://doi.org/10.1097/00000658-194007000-00016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Henriques, C. Q. (1962). The veins of the vertebral column and their role in the spread of cancer. Annals of the Royal College of Surgeons of England, 31(1), 1–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Chiang, S. P. H., Cabrera, R. M., & Segall, J. E. (2016). Tumor cell intravasation. American Journal of Physiology. Cellular Physiology, 311(1), C1–C14. https://doi.org/10.1152/ajpcell.00238.2015.

    Article  Google Scholar 

  26. Valastyan, S., & Weinberg, R. A. (2011). Tumor metastasis: molecular insights and evolving paradigms. Cell, 147(2), 275–292. https://doi.org/10.1016/j.cell.2011.09.024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Grignon, D. J. (2018). Prostate cancer reporting and staging: needle biopsy and radical prostatectomy specimens. Modern Pathology, 31(S1), S96–S109. https://doi.org/10.1038/modpathol.2017.167.

  28. Fleshner, K., Assel, M., Benfante, N., Lee, J., Vickers, A., Fine, S., et al. (2016). Clinical findings and treatment outcomes in patients with extraprostatic extension identified on prostate biopsy. The Journal of Urology, 196(3), 703–708. https://doi.org/10.1016/j.juro.2016.03.152.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Mikel Hubanks, J., Boorjian, S. A., Frank, I., Gettman, M. T., Houston Thompson, R., Rangel, L. J., et al. (2014). The presence of extracapsular extension is associated with an increased risk of death from prostate cancer after radical prostatectomy for patients with seminal vesicle invasion and negative lymph nodes. Urologic Oncology, 32(1), 26.e21–26.e27. https://doi.org/10.1016/j.urolonc.2012.09.002.

    Article  Google Scholar 

  30. De Vivar, A. D., Sayeeduddin, M., Rowley, D., Cubilla, A., Miles, B., Kadmon, D., et al. (2017). Histologic features of stromogenic carcinoma of the prostate (carcinomas with reactive stroma grade 3). Human Pathology, 63, 202–211. https://doi.org/10.1016/j.humpath.2017.02.019.

    Article  PubMed  Google Scholar 

  31. Au, S. H., Storey, B. D., Moore, J. C., Tang, Q., Chen, Y. L., Javaid, S., et al. (2016). Clusters of circulating tumor cells traverse capillary-sized vessels. Proceedings of the National Academy of Sciences of the United States of America. https://doi.org/10.1073/pnas.1524448113.

  32. Rubenstein, C. S., Gard, J. M. C., Wang, M., McGrath, J. E., Ingabire, N., Hinton, J. P., et al. (2019). Gene editing of alpha6 integrin inhibits muscle invasive networks and increases cell-cell biophysical properties in prostate cancer. Cancer Research, 79(18), 4703–4714. https://doi.org/10.1158/0008-5472.Can-19-0868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Magi-Galluzzi, C., Evans, A. J., Delahunt, B., Epstein, J. I., Griffiths, D. F., van der Kwast, T. H., et al. (2011). International Society of Urological Pathology (ISUP) Consensus conference on handling and staging of radical prostatectomy specimens. Working group 3: extraprostatic extension, lymphovascular invasion and locally advanced disease. Modern Pathology, 24(1), 26–38. https://doi.org/10.1038/modpathol.2010.158.

    Article  PubMed  Google Scholar 

  34. Fine, S. W., Amin, M. B., Berney, D. M., Bjartell, A., Egevad, L., Epstein, J. I., et al. (2012). A contemporary update on pathology reporting for prostate cancer: biopsy and radical prostatectomy specimens. European Urology, 62(1), 20–39. https://doi.org/10.1016/j.eururo.2012.02.055.

    Article  PubMed  Google Scholar 

  35. Ball, M. W., Partin, A. W., & Epstein, J. I. (2015). Extent of extraprostatic extension independently influences biochemical recurrence-free survival: evidence for further pT3 subclassification. Urology, 85(1), 161–164. https://doi.org/10.1016/j.urology.2014.08.025.

    Article  PubMed  Google Scholar 

  36. Miller, J. S., Chen, Y., Ye, H., Robinson, B. D., Brimo, F., & Epstein, J. I. (2010). Extraprostatic extension of prostatic adenocarcinoma on needle core biopsy: report of 72 cases with clinical follow-up. BJU International, 106(3), 330–333. https://doi.org/10.1111/j.1464-410X.2009.09110.x.

    Article  PubMed  Google Scholar 

  37. Shieh, A. C., Guler, E., Ojili, V., Paspulati, R. M., Elliott, R., Ramaiya, N. H., et al. (2020). Extraprostatic extension in prostate cancer: primer for radiologists. Abdom Radiol (NY), https://doi.org/10.1007/s00261-020-02555-x.

    Book  Google Scholar 

  38. Society, A. C. (2020). Survival Rates for Bladder Cancer. https://www.cancer.org/cancer/bladder-cancer/detection-diagnosis-staging/survival-rates.html. Accessed April 5 2020.

  39. Institute., N. C. (2018). Bladder Cancer. https://training.seer.cancer.gov/bladder/. Accessed May 11 2020.

  40. Maj, M., Kokocha, A., Bajek, A., & Drewa, T. (2018). The interplay between adipose-derived stem cells and bladder cancer cells. Scientific Reports, 8(1), 15118. https://doi.org/10.1038/s41598-018-33397-9.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hariharan, N., Ashcraft, K. A., Svatek, R. S., Livi, C. B., Wilson, D., Kaushik, D., et al. (2018). Adipose tissue-secreted factors alter bladder cancer cell migration. J Obesity, 2018, 9247864, https://doi.org/10.1155/2018/9247864.

  42. Ross, J. S., del Rosario, A. D., Figge, H. L., Sheehan, C., Fisher, H. A., & Bui, H. X. (1995). E-cadherin expression in papillary transitional cell carcinoma of the urinary bladder. Human Pathology, 26(9), 940–944, doi:https://doi.org/10.1016/0046-8177(95)90081-0.

  43. Xie, Y., Li, P., Gao, Y., Gu, L., Chen, L., Fan, Y., et al. (2017). Reduced E-cadherin expression is correlated with poor prognosis in patients with bladder cancer: a systematic review and meta-analysis. Oncotarget, 8(37), 62489–62499, doi:https://doi.org/10.18632/oncotarget.19934.

  44. Camp, E. R., Patterson, L. D., Kester, M., & Voelkel-Johnson, C. (2017). Therapeutic implications of bioactive sphingolipids: a focus on colorectal cancer. Cancer Biology & Therapy, 18(9), 640–650. https://doi.org/10.1080/15384047.2017.1345396.

    Article  CAS  Google Scholar 

  45. Godlewski, J., & Kmiec, Z. (2020). Colorectal cancer invasion and atrophy of the enteric nervous system: potential feedback and impact on cancer progression. International Journal of Molecular Sciences, 21(9). https://doi.org/10.3390/ijms21093391.

  46. Li, S. S., Xu, L. Z., Zhou, W., Yao, S., Wang, C. L., Xia, J. L., et al. (2017). p62/SQSTM1 interacts with vimentin to enhance breast cancer metastasis. Carcinogenesis, 38(11), 1092–1103. https://doi.org/10.1093/carcin/bgx099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Takatsuna, M., Morohashi, S., Yoshizawa, T., Hirai, H., Haga, T., Ota, R., et al. (2016). Myofibroblasts of the muscle layer stimulate the malignant potential of colorectal cancer. Oncology Reports, 36(3), 1251–1257. https://doi.org/10.3892/or.2016.4932.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ueno, H., Hase, K., Hashiguchi, Y., Ishiguro, M., Kajiwara, Y., Shimazaki, H., et al. (2009). Growth pattern in the muscular layer reflects the biological behaviour of colorectal cancer. Colorectal Disease, 11(9), 951–959. https://doi.org/10.1111/j.1463-1318.2008.01718.x.

    Article  CAS  PubMed  Google Scholar 

  49. Ayala, G., Tuxhorn, J. A., Wheeler, T. M., Frolov, A., Scardino, P. T., Ohori, M., et al. (2003). Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clinical Cancer Research, 9(13), 4792–4801.

    CAS  PubMed  Google Scholar 

  50. Cordon-Cardo, C. (2008). Molecular alterations associated with bladder cancer initiation and progression. Scandinavian Journal of Urology and Nephrology. Supplementum, (218), 154–165. https://doi.org/10.1080/03008880802291915.

  51. Hasui, Y., Osada, Y., Kitada, S., & Nishi, S. (1994). Significance of invasion to the muscularis mucosae on the progression of superficial bladder cancer. Urology, 43(6), 782–786. https://doi.org/10.1016/0090-4295(94)90134-1.

    Article  CAS  PubMed  Google Scholar 

  52. Ross, J. S., Del Rosario, A. D., Figge, H. L., Sheehan, C., Fisher, H. A. G., & Bui, H. X. (1995). E-cadherin expression in papillary transitional cell carcinoma of the urinary bladder. Human Pathology, 26(9), 940–944. https://doi.org/10.1016/0046-8177(95)90081-0.

    Article  CAS  PubMed  Google Scholar 

  53. Wong, Y. C., & Tam, N. N. (2002). Dedifferentiation of stromal smooth muscle as a factor in prostate carcinogenesis. Differentiation, 70(9–10), 633–645. https://doi.org/10.1046/j.1432-0436.2002.700916.x.

    Article  CAS  PubMed  Google Scholar 

  54. Kugler, R., Mietens, A., Seidensticker, M., Tasch, S., Wagenlehner, F. M., Kaschtanow, A., et al. (2018). Novel imaging of the prostate reveals spontaneous gland contraction and excretory duct quiescence together with different drug effects. The FASEB Journal, 32(3), 1130–1138. https://doi.org/10.1096/fj.201700430R.

    Article  PubMed  Google Scholar 

  55. Andersson, K. E., & Arner, A. (2004). Urinary bladder contraction and relaxation: Physiology and pathophysiology. Physiological Reviews, 84(3), 935–986. https://doi.org/10.1152/physrev.00038.2003.

    Article  CAS  PubMed  Google Scholar 

  56. Fry, C. H., Meng, E., & Young, J. S. (2010). The physiological function of lower urinary tract smooth muscle. Autonomic Neuroscience, 154(1–2), 3–13. https://doi.org/10.1016/j.autneu.2009.10.006.

    Article  CAS  PubMed  Google Scholar 

  57. Peinetti, N., Scalerandi, M. V., Cuello Rubio, M. M., Leimgruber, C., Nicola, J. P., Torres, A. I., et al. (2018). The response of prostate smooth muscle cells to testosterone is determined by the subcellular distribution of the androgen receptor. Endocrinology, 159(2), 945–956. https://doi.org/10.1210/en.2017-00718.

    Article  CAS  PubMed  Google Scholar 

  58. Hristov, K. L., Parajuli, S. P., Provence, A., & Petkov, G. V. (2016). Testosterone decreases urinary bladder smooth muscle excitability via novel signaling mechanism involving direct activation of the BK channels. American Journal of Physiology. Renal Physiology, 311(6), F1253–f1259. https://doi.org/10.1152/ajprenal.00238.2016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. University, R. (2016). Smooth muscle. In Anatomy and Physiology (pp. 932–940): OpenStax CNX.

  60. Hafen, B. B., & Burns, B. (2020, Jan-). Physiology, Smooth muscle. In StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing LLC.

  61. Burkin, D. J., & Kaufman, S. J. (1999). The alpha7beta1 integrin in muscle development and disease. Cell and Tissue Research, 296(1), 183–190. https://doi.org/10.1007/s004410051279.

    Article  CAS  PubMed  Google Scholar 

  62. Boppart, M. D., Burkin, D. J., & Kaufman, S. J. (2006). Alpha7beta1-integrin regulates mechanotransduction and prevents skeletal muscle injury. American Journal of Physiology. Cell Physiology, 290(6), C1660–C1665. https://doi.org/10.1152/ajpcell.00317.2005.

    Article  CAS  PubMed  Google Scholar 

  63. Jung, J., Ahn, H. K., & Huh, Y. (2012). Clinical and functional anatomy of the urethral sphincter. International Neurourology Journal, 16(3), 102–106. https://doi.org/10.5213/inj.2012.16.3.102.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Cox, T. R., & Erler, J. T. (2011). Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Disease Models & Mechanisms, 4(2), 165–178. https://doi.org/10.1242/dmm.004077.

    Article  CAS  Google Scholar 

  65. Changede, R., & Sheetz, M. (2017). Integrin and cadherin clusters: a robust way to organize adhesions for cell mechanics. Bioessays, 39(1), 1–12. https://doi.org/10.1002/bies.201600123.

    Article  CAS  PubMed  Google Scholar 

  66. Goodwin, K., Ellis, S. J., Lostchuck, E., Zulueta-Coarasa, T., Fernandez-Gonzalez, R., & Tanentzapf, G. (2016). Basal cell-extracellular matrix adhesion regulates force transmission during tissue morphogenesis. Developmental Cell, 39(5), 611–625. https://doi.org/10.1016/j.devcel.2016.11.003.

    Article  CAS  PubMed  Google Scholar 

  67. Mui, K. L., Chen, C. S., & Assoian, R. K. (2016). The mechanical regulation of integrin-cadherin crosstalk organizes cells. signaling and forces. J Cell Sci, 129(6), 1093–1100. https://doi.org/10.1242/jcs.183699.

    Article  CAS  PubMed  Google Scholar 

  68. Okada, H., Lai, N. C., Kawaraguchi, Y., Liao, P., Copps, J., Sugano, Y., et al. (2013). Integrins protect cardiomyocytes from ischemia/reperfusion injury. The Journal of Clinical Investigation, 123(10), 4294–4308. https://doi.org/10.1172/jci64216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Liu, J., Xu, W., Sun, T., Wang, F., Puscheck, E., Brigstock, D., et al. (2009). Hyperosmolar stress induces global mRNA responses in placental trophoblast stem cells that emulate early post-implantation differentiation. Placenta, 30(1), 66–73. https://doi.org/10.1016/j.placenta.2008.10.009.

    Article  PubMed  Google Scholar 

  70. Yuzhalin, A. E., Lim, S. Y., Kutikhin, A. G., & Gordon-Weeks, A. N. (2018). Dynamic matrisome: ECM remodeling factors licensing cancer progression and metastasis. Biochimica Et Biophysica Acta. Reviews on Cancer, 1870(2), 207–228. https://doi.org/10.1016/j.bbcan.2018.09.002.

    Article  CAS  PubMed  Google Scholar 

  71. Cheng, L., Montironi, R., Davidson, D. D., & Lopez-Beltran, A. (2009). Staging and reporting of urothelial carcinoma of the urinary bladder. Modern Pathology, 22(Suppl 2), S70–S95. https://doi.org/10.1038/modpathol.2009.1.

    Article  PubMed  Google Scholar 

  72. Weigelin, B., Bakker, G. J., & Friedl, P. (2012). Intravital third harmonic generation microscopy of collective melanoma cell invasion: Principles of interface guidance and microvesicle dynamics. Intravital, 1(1), 32–43. https://doi.org/10.4161/intv.21223.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Layke, J. C., & Lopez, P. P. (2004). Gastric cancer: diagnosis and treatment options. American Family Physician, 69(5), 1133–1140.

    PubMed  Google Scholar 

  74. Andkhoie, M., Meyer, D., & Szafron, M. (2018). Factors underlying treatment decision-making for localized prostate cancer in the U.S. and Canada: a scoping review using principal component analysis. Canadian Urological Association journal = Journal de l'Association des urologues du Canada, 13(7), E220–E225. https://doi.org/10.5489/cuaj.5538.

    Article  PubMed Central  Google Scholar 

  75. Cunha, G. R., Hayward, S. W., Dahiya, R., & Foster, B. A. (1996). Smooth muscle-epithelial interactions in normal and neoplastic prostatic development. Acta Anatomica (Basel), 155(1), 63–72. https://doi.org/10.1159/000147791.

    Article  CAS  Google Scholar 

  76. Olumi, A. F., Grossfeld, G. D., Hayward, S. W., Carroll, P. R., Tlsty, T. D., & Cunha, G. R. (1999). Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Research, 59(19), 5002–5011. https://doi.org/10.1186/bcr138.

    Article  CAS  PubMed  Google Scholar 

  77. Wang, Y., Li, Y., Chen, Z., Wang, T., Gu, J., Wu, X., et al. (2017). The evaluation of colorectal cancer risk in serum by anti-DESMIN-conjugated CdTe/CdS quantum dots. Clinical Laboratory, 63(3), 579–586. https://doi.org/10.7754/Clin.Lab.2016.161005.

    Article  CAS  PubMed  Google Scholar 

  78. Zhang, F., Hao, F., An, D., Zeng, L., Wang, Y., Xu, X., et al. (2015). The matricellular protein Cyr61 is a key mediator of platelet-derived growth factor-induced cell migration. The Journal of Biological Chemistry, 290(13), 8232–8242. https://doi.org/10.1074/jbc.M114.623074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Yang, R., Chen, Y., & Chen, D. (2018). Biological functions and role of CCN1/Cyr61 in embryogenesis and tumorigenesis in the female reproductive system (review). Molecular Medicine Reports, 17(1), 3–10. https://doi.org/10.3892/mmr.2017.7880.

    Article  CAS  PubMed  Google Scholar 

  80. Landowski, T. H., Gard, J., Pond, E., Pond, G. D., Nagle, R. B., Geffre, C. P., et al. (2014). Targeting integrin α6 stimulates curative-type bone metastasis lesions in a xenograft model. Molecular Cancer Therapeutics, 13(6), 1558–1566. https://doi.org/10.1158/1535-7163.Mct-13-0962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Sutoh Yoneyama, M., Hatakeyama, S., Habuchi, T., Inoue, T., Nakamura, T., Funyu, T., et al. (2014). Vimentin intermediate filament and plectin provide a scaffold for invadopodia, facilitating cancer cell invasion and extravasation for metastasis. European Journal of Cell Biology, 93(4), 157–169. https://doi.org/10.1016/j.ejcb.2014.03.002.

  82. Friedl, P., Locker, J., Sahai, E., & Segall, J. E. (2012). Classifying collective cancer cell invasion. Nature Cell Biology, 14(8), 777–783. https://doi.org/10.1038/ncb2548.

    Article  PubMed  Google Scholar 

  83. Imanishi, K., Yoneyama, M. S., Hatakeyama, S., Yamamoto, H., Koie, T., Saitoh, H., et al. (2014). Invadopodia are essential in transurothelial invasion during the muscle invasion of bladder cancer cells. Molecular Medicine Reports, 9(6), 2159–2165. https://doi.org/10.3892/mmr.2014.2113.

    Article  CAS  PubMed  Google Scholar 

  84. Scher, H. I., & Pantel, K. (2009). Bone marrow aspiration for disseminated tumor cell detection: A must-have test or is the jury still out? Journal of Clinical Oncology, 27(10), 1531–1533. https://doi.org/10.1200/jco.2008.21.2092.

    Article  PubMed  Google Scholar 

  85. van der Toom, E. E., Verdone, J. E., & Pienta, K. J. (2016). Disseminated tumor cells and dormancy in prostate cancer metastasis. Current Opinion in Biotechnology, 40, 9–15. https://doi.org/10.1016/j.copbio.2016.02.002.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Morgan, T. M., Lange, P. H., Porter, M. P., Lin, D. W., Ellis, W. J., Gallaher, I. S., et al. (2009). Disseminated tumor cells in prostate cancer patients after radical prostatectomy and without evidence of disease predicts biochemical recurrence. Clinical Cancer Research, 15(2), 677–683. https://doi.org/10.1158/1078-0432.ccr-08-1754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Aceto, N., Bardia, A., Miyamoto, D. T., Donaldson, M. C., Wittner, B. S., Spencer, J. A., et al. (2014). Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell, 158(5), 1110–1122. https://doi.org/10.1016/j.cell.2014.07.013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Cheung, K. J., Padmanaban, V., Silvestri, V., Schipper, K., Cohen, J. D., Fairchild, A. N., et al. (2016). Polyclonal breast cancer metastases arise from collective dissemination of keratin 14-expressing tumor cell clusters. Proceedings of the National Academy of Sciences of the United States of America, 113(7), E854–E863. https://doi.org/10.1073/pnas.1508541113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Mayor, R., & Etienne-Manneville, S. (2016). The front and rear of collective cell migration. Nature Reviews. Molecular Cell Biology, 17(2), 97–109. https://doi.org/10.1038/nrm.2015.14.

    Article  CAS  PubMed  Google Scholar 

  90. Aceto, N., Toner, M., Maheswaran, S., & Haber, D. A. (2015). En route to metastasis: circulating tumor cell clusters and epithelial-to-mesenchymal transition. Trends Cancer, 1(1), 44–52. https://doi.org/10.1016/j.trecan.2015.07.006.

    Article  PubMed  Google Scholar 

  91. Kremer, C. L., Schmelz, M., & Cress, A. E. (2006). Integrin-dependent amplification of the G2 arrest induced by ionizing radiation. Prostate, 66(1), 88–96. https://doi.org/10.1002/pros.20316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Harryman, W. L., Hinton, J. P., Rubenstein, C. P., Singh, P., Nagle, R. B., Parker, S. J., et al. (2016). The cohesive metastasis phenotype in human prostate cancer. Biochimica et Biophysica Acta, 1866(2), 221–231. https://doi.org/10.1016/j.bbcan.2016.09.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Ross, T. D., Coon, B. G., Yun, S., Baeyens, N., Tanaka, K., Ouyang, M., et al. (2013). Integrins in mechanotransduction. Current Opinion in Cell Biology, 25(5), 613–618. https://doi.org/10.1016/j.ceb.2013.05.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell, 126(4), 677–689. https://doi.org/10.1016/j.cell.2006.06.044.

    Article  CAS  PubMed  Google Scholar 

  95. Orr, A. W., Helmke, B. P., Blackman, B. R., & Schwartz, M. A. (2006). Mechanisms of mechanotransduction. Developmental Cell, 10(1), 11–20. https://doi.org/10.1016/j.devcel.2005.12.006.

    Article  CAS  PubMed  Google Scholar 

  96. Lu, P., Weaver, V. M., & Werb, Z. (2012). The extracellular matrix: a dynamic niche in cancer progression. The Journal of Cell Biology, 196(4), 395–406. https://doi.org/10.1083/jcb.201102147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Knox, J. D., Cress, A. E., Clark, V., Manriquez, L., Affinito, K. S., Dalkin, B. L., et al. (1994). Differential expression of extracellular matrix molecules and the alpha 6-integrins in the normal and neoplastic prostate. The American Journal of Pathology, 145(1), 167–174.

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Nagle, R. B., Hao, J., Knox, J. D., Dalkin, B. L., Clark, V., & Cress, A. E. (1995). Expression of hemidesmosomal and extracellular matrix proteins by normal and malignant human prostate tissue. The American Journal of Pathology, 146(6), 1498–1507.

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Wang, M., Nagle, R. B., Knudsen, B. S., Rogers, G. C., & Cress, A. E. (2017). A basal cell defect promotes budding of prostatic intraepithelial neoplasia. Journal of Cell Science, 130(1), 104–110. https://doi.org/10.1242/jcs.188177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Bonkhoff, H., & Remberger, K. (1996). Differentiation pathways and histogenetic aspects of normal and abnormal prostatic growth: a stem cell model. Prostate, 28(2), 98–106. https://doi.org/10.1002/(sici)1097-0045(199602)28:2<98::Aid-pros4>3.0.Co;2-j.

    Article  CAS  PubMed  Google Scholar 

  101. Mosquera, J. M., Perner, S., Genega, E. M., Sanda, M., Hofer, M. D., Mertz, K. D., et al. (2008). Characterization of TMPRSS2-ERG fusion high-grade prostatic intraepithelial neoplasia and potential clinical implications. Clinical Cancer Research, 14(11), 3380–3385. https://doi.org/10.1158/1078-0432.Ccr-07-5194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Iwata, T., Schultz, D., Hicks, J., Hubbard, G. K., Mutton, L. N., Lotan, T. L., et al. (2010). MYC overexpression induces prostatic intraepithelial neoplasia and loss of Nkx3.1 in mouse luminal epithelial cells. PLoS One, 5(2), e9427. https://doi.org/10.1371/journal.pone.0009427.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Petein, M., Michel, P., van Velthoven, R., Pasteels, J. L., Brawer, M. K., Davis, J. R., et al. (1991). Morphonuclear relationship between prostatic intraepithelial neoplasia and cancers as assessed by digital cell image analysis. American Journal of Clinical Pathology, 96(5), 628–634. https://doi.org/10.1093/ajcp/96.5.628.

    Article  CAS  PubMed  Google Scholar 

  104. Pfeifer, C. R., Irianto, J., & Discher, D. E. (2019). Nuclear mechanics and cancer cell migration. Advances in Experimental Medicine and Biology, 1146, 117–130. https://doi.org/10.1007/978-3-030-17593-1_8.

    Article  CAS  PubMed  Google Scholar 

  105. Jansen, K. A., Donato, D. M., Balcioglu, H. E., Schmidt, T., Danen, E. H., & Koenderink, G. H. (2015). A guide to mechanobiology: where biology and physics meet. Biochimica et Biophysica Acta, 1853(11 Pt B), 3043–3052. https://doi.org/10.1016/j.bbamcr.2015.05.007.

    Article  CAS  PubMed  Google Scholar 

  106. Chen, Y., Ju, L., Rushdi, M., Ge, C., & Zhu, C. (2017). Receptor-mediated cell mechanosensing. Molecular Biology of the Cell, 28(23), 3134–3155. https://doi.org/10.1091/mbc.E17-04-0228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Kechagia, J. Z., Ivaska, J., & Roca-Cusachs, P. (2019). Integrins as biomechanical sensors of the microenvironment. Nature Reviews. Molecular Cell Biology, 20(8), 457–473. https://doi.org/10.1038/s41580-019-0134-2.

    Article  CAS  PubMed  Google Scholar 

  108. Panzetta, V., Fusco, S., & Netti, P. A. (2019). Cell mechanosensing is regulated by substrate strain energy rather than stiffness. Proceedings of the National Academy of Sciences of the United States of America, 116(44), 22004–22013. https://doi.org/10.1073/pnas.1904660116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Geiger, B., Bershadsky, A., Pankov, R., & Yamada, K. M. (2001). Transmembrane crosstalk between the extracellular matrix--cytoskeleton crosstalk. Nature Reviews. Molecular Cell Biology, 2(11), 793–805. https://doi.org/10.1038/35099066.

    Article  CAS  PubMed  Google Scholar 

  110. Kobayashi, T., & Sokabe, M. (2010). Sensing substrate rigidity by mechanosensitive ion channels with stress fibers and focal adhesions. Current Opinion in Cell Biology, 22(5), 669–676. https://doi.org/10.1016/j.ceb.2010.08.023.

    Article  CAS  PubMed  Google Scholar 

  111. Janoštiak, R., Pataki, A. C., Brábek, J., & Rösel, D. (2014). Mechanosensors in integrin signaling: the emerging role of p130Cas. European Journal of Cell Biology, 93(10–12), 445–454. https://doi.org/10.1016/j.ejcb.2014.07.002.

    Article  PubMed  Google Scholar 

  112. Changede, R., Cai, H., Wind, S. J., & Sheetz, M. P. (2019). Integrin nanoclusters can bridge thin matrix fibres to form cell-matrix adhesions. Nature Materials, 18(12), 1366–1375. https://doi.org/10.1038/s41563-019-0460-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Weber, G. F., Bjerke, M. A., & DeSimone, D. W. (2011). Integrins and cadherins join forces to form adhesive networks. Journal of Cell Science, 124(Pt 8), 1183–1193. https://doi.org/10.1242/jcs.064618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Yap, A. S., Duszyc, K., & Viasnoff, V. (2018). Mechanosensing and Mechanotransduction at cell-cell junctions. Cold Spring Harbor Perspectives in Biology, 10(8). https://doi.org/10.1101/cshperspect.a028761.

  115. Huveneers, S., & de Rooij, J. (2013). Mechanosensitive systems at the cadherin-F-actin interface. Journal of Cell Science, 126(Pt 2), 403–413. https://doi.org/10.1242/jcs.109447.

    Article  CAS  PubMed  Google Scholar 

  116. Lecuit, T., & Yap, A. S. (2015). E-cadherin junctions as active mechanical integrators in tissue dynamics. Nature Cell Biology, 17(5), 533–539. https://doi.org/10.1038/ncb3136.

    Article  CAS  PubMed  Google Scholar 

  117. Barry, A. K., Wang, N., & Leckband, D. E. (2015). Local VE-cadherin mechanotransduction triggers long-ranged remodeling of endothelial monolayers. Journal of Cell Science, 128(7), 1341–1351. https://doi.org/10.1242/jcs.159954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Maître, J. L., Berthoumieux, H., Krens, S. F., Salbreux, G., Jülicher, F., Paluch, E., et al. (2012). Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science, 338(6104), 253–256. https://doi.org/10.1126/science.1225399.

    Article  PubMed  Google Scholar 

  119. Horton, E. R., Humphries, J. D., James, J., Jones, M. C., Askari, J. A., & Humphries, M. J. (2016). The integrin adhesome network at a glance. Journal of Cell Science, 129(22), 4159–4163. https://doi.org/10.1242/jcs.192054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Nishiuchi, R., Takagi, J., Hayashi, M., Ido, H., Yagi, Y., Sanzen, N., et al. (2006). Ligand-binding specificities of laminin-binding integrins: a comprehensive survey of laminin-integrin interactions using recombinant alpha3beta1, alpha6beta1, alpha7beta1 and alpha6beta4 integrins. Matrix Biology, 25(3), 189–197. https://doi.org/10.1016/j.matbio.2005.12.001.

    Article  CAS  PubMed  Google Scholar 

  121. Lengyel, E., Makowski, L., DiGiovanni, J., & Kolonin, M. G. (2018). Cancer as a matter of fat: the crosstalk between adipose tissue and tumors. Trends Cancer, 4(5), 374–384. https://doi.org/10.1016/j.trecan.2018.03.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Modesitt, S. C., Hsu, J. Y., Chowbina, S. R., Lawrence, R. T., & Hoehn, K. L. (2012). Not all fat is equal: differential gene expression and potential therapeutic targets in subcutaneous adipose, visceral adipose, and endometrium of obese women with and without endometrial cancer. International Journal of Gynecological Cancer, 22(5), 732–741. https://doi.org/10.1097/IGC.0b013e3182510496.

    Article  PubMed  Google Scholar 

  123. Saely, C. H., Geiger, K., & Drexel, H. (2012). Brown versus white adipose tissue: a mini-review. Gerontology, 58(1), 15–23. https://doi.org/10.1159/000321319.

    Article  PubMed  Google Scholar 

  124. Cozzo, A. J., Fuller, A. M., & Makowski, L. (2017). Contribution of adipose tissue to development of cancer. Comprehensive Physiology, 8(1), 237–282. https://doi.org/10.1002/cphy.c170008.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Lauby-Secretan, B., Scoccianti, C., Loomis, D., Grosse, Y., Bianchini, F., Straif, K., et al. (2016). Body fatness and cancer--viewpoint of the IARC working group. The New England Journal of Medicine, 375(8), 794–798. https://doi.org/10.1056/NEJMsr1606602.

    Article  PubMed  PubMed Central  Google Scholar 

  126. Steele, C. B., Thomas, C. C., Henley, S. J., Massetti, G. M., Galuska, D. A., Agurs-Collins, T., et al. (2017). Vital signs: trends in incidence of cancers associated with overweight and obesity - United States, 2005–2014. MMWR. Morbidity and Mortality Weekly Report, 66(39), 1052–1058. https://doi.org/10.15585/mmwr.mm6639e1.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Quail, D. F., & Dannenberg, A. J. (2019). The obese adipose tissue microenvironment in cancer development and progression. Nature Reviews. Endocrinology, 15(3), 139–154. https://doi.org/10.1038/s41574-018-0126-x.

    Article  PubMed  PubMed Central  Google Scholar 

  128. Nieman, K. M., Kenny, H. A., Penicka, C. V., Ladanyi, A., Buell-Gutbrod, R., Zillhardt, M. R., et al. (2011). Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nature Medicine, 17(11), 1498–1503. https://doi.org/10.1038/nm.2492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zhao, P., & Zhang, Z. (2018). TNF-α promotes colon cancer cell migration and invasion by upregulating TROP-2. Oncology Letters, 15(3), 3820–3827. https://doi.org/10.3892/ol.2018.7735.

    Article  PubMed  PubMed Central  Google Scholar 

  130. Song, X., Voronov, E., Dvorkin, T., Fima, E., Cagnano, E., Benharroch, D., et al. (2003). Differential effects of IL-1 alpha and IL-1 beta on tumorigenicity patterns and invasiveness. Journal of Immunology, 171(12), 6448–6456. https://doi.org/10.4049/jimmunol.171.12.6448.

    Article  CAS  Google Scholar 

  131. Nguyen, D. P., Li, J., & Tewari, A. K. (2014). Inflammation and prostate cancer: the role of interleukin 6 (IL-6). BJU International, 113(6), 986–992. https://doi.org/10.1111/bju.12452.

    Article  CAS  PubMed  Google Scholar 

  132. Ham, I. H., Oh, H. J., Jin, H., Bae, C. A., Jeon, S. M., Choi, K. S., et al. (2019). Targeting interleukin-6 as a strategy to overcome stroma-induced resistance to chemotherapy in gastric cancer. Molecular Cancer, 18(1), 68. https://doi.org/10.1186/s12943-019-0972-8.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Zhang, T., Tseng, C., Zhang, Y., Sirin, O., Corn, P. G., Li-Ning-Tapia, E. M., et al. (2016). CXCL1 mediates obesity-associated adipose stromal cell trafficking and function in the tumour microenvironment. Nature Communications, 7, 11674. https://doi.org/10.1038/ncomms11674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Gao, Z., Daquinag, A. C., Su, F., Snyder, B., & Kolonin, M. G. (2018). PDGFRα/PDGFRβ signaling balance modulates progenitor cell differentiation into white and beige adipocytes. Development, 145(1). https://doi.org/10.1242/dev.155861.

  135. Curat, C. A., Wegner, V., Sengenès, C., Miranville, A., Tonus, C., Busse, R., et al. (2006). Macrophages in human visceral adipose tissue: Increased accumulation in obesity and a source of resistin and visfatin. Diabetologia, 49(4), 744–747. https://doi.org/10.1007/s00125-006-0173-z.

    Article  CAS  PubMed  Google Scholar 

  136. Camp, S. M., Ceco, E., Evenoski, C. L., Danilov, S. M., Zhou, T., Chiang, E. T., et al. (2015). Unique toll-like receptor 4 activation by NAMPT/PBEF induces NFκB signaling and inflammatory lung injury. Scientific Reports, 5, 13135. https://doi.org/10.1038/srep13135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Audrito, V., Serra, S., Brusa, D., Mazzola, F., Arruga, F., Vaisitti, T., et al. (2015). Extracellular nicotinamide phosphoribosyltransferase (NAMPT) promotes M2 macrophage polarization in chronic lymphocytic leukemia. Blood, 125(1), 111–123. https://doi.org/10.1182/blood-2014-07-589069.

    Article  CAS  PubMed  Google Scholar 

  138. Hellsten, R., Lilljebjörn, L., Johansson, M., Leandersson, K., & Bjartell, A. (2019). The STAT3 inhibitor galiellalactone inhibits the generation of MDSC-like monocytes by prostate cancer cells and decreases immunosuppressive and tumorigenic factors. Prostate, 79(14), 1611–1621. https://doi.org/10.1002/pros.23885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Samal, B., Sun, Y., Stearns, G., Xie, C., Suggs, S., & McNiece, I. (1994). Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Molecular and Cellular Biology, 14(2), 1431–1437. https://doi.org/10.1128/mcb.14.2.1431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Trayhurn, P., & Wood, I. S. (2004). Adipokines: Inflammation and the pleiotropic role of white adipose tissue. The British Journal of Nutrition, 92(3), 347–355. https://doi.org/10.1079/bjn20041213.

    Article  CAS  PubMed  Google Scholar 

  141. Sun, B. L., Sun, X., Casanova, N., Garcia, A. N., Oita, R., Algotar, A. M., et al. (2020). Role of secreted extracellular nicotinamide phosphoribosyltransferase (eNAMPT) in prostate cancer progression: novel biomarker and therapeutic target. EBioMedicine, 61, 103059. https://doi.org/10.1016/j.ebiom.2020.103059.

    Article  PubMed  Google Scholar 

  142. Nieman, K. M., Romero, I. L., Van Houten, B., & Lengyel, E. (2013). Adipose tissue and adipocytes support tumorigenesis and metastasis. Biochimica et Biophysica Acta, 1831(10), 1533–1541, doi:https://doi.org/10.1016/j.bbalip.2013.02.010.

  143. Kapoor, J., Namdarian, B., Pedersen, J., Hovens, C., Moon, D., Peters, J., et al. (2013). Extraprostatic extension into periprostatic fat is a more important determinant of prostate cancer recurrence than an invasive phenotype. The Journal of Urology, 190(6), 2061–2066. https://doi.org/10.1016/j.juro.2013.06.050.

    Article  PubMed  Google Scholar 

  144. Ribeiro, R., Monteiro, C., Cunha, V., Oliveira, M. J., Freitas, M., Fraga, A., et al. (2012). Human periprostatic adipose tissue promotes prostate cancer aggressiveness in vitro. Journal of Experimental & Clinical Cancer Research, 31(1), 32. https://doi.org/10.1186/1756-9966-31-32.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge staff support of the Tissue Acquisition and Cellular/Molecular Analysis Resource at the University of Arizona Cancer Center and the funding sources that made the work possible, including NIH-NCI T32CA009213 (to A.E. Cress), NIH-NHLBI P01 HL126609 (to J.G.N. Garcia), Project 3 (to A.E. Cress), NCI-P30 CA 23074, and F30 CA247106 to K.D. Marr.

Code availability

N/A

Funding

The work was supported by the National Cancer Institute of the National Institutes of Health under award numbers P30 CA023074 and F30 CA247106.

Author information

Authors and Affiliations

  1. Department of Cellular and Molecular Medicine, The University of Arizona Cancer Center, 1515 N. Campbell Ave., Tucson, AZ, 85724, USA

    William L. Harryman, Kendra D. Marr, Daniel Hernandez-Cortes, Raymond B. Nagle, Joe G. N. Garcia & Anne E. Cress

Authors
  1. William L. Harryman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kendra D. Marr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel Hernandez-Cortes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Raymond B. Nagle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joe G. N. Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anne E. Cress
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Anne E. Cress conceptualized the article; William L. Harryman and Anne E. Cress did the literature search; William L. Harryman and Anne E. Cress did the writing; Raymond B. Nagle, Kendra D. Marr, Daniel Hernandez-Cortes, and Joe G.N. Garcia critically evaluated and edited the article adding content prior to submission.

Corresponding author

Correspondence to Anne E. Cress.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

N/A

Consent to participate

N/A

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harryman, W.L., Marr, K.D., Hernandez-Cortes, D. et al. Cohesive cancer invasion of the biophysical barrier of smooth muscle. Cancer Metastasis Rev 40, 205–219 (2021). https://doi.org/10.1007/s10555-020-09950-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-020-09950-2

Keywords

Search

Navigation